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  • 1. Benavides, Mar
    et al.
    Caffin, Mathieu
    Duhamel, Solange
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Grosso, Olivier
    Guieu, Cécile
    Van Wambeke, France
    Bonnet, Sophie
    Anomalously high abundance of Crocosphaera in the South Pacific Gyre2022In: FEMS Microbiology Letters, ISSN 0378-1097, E-ISSN 1574-6968, Vol. 369, no 1, article id fnac039Article in journal (Refereed)
    Abstract [en]

    The unicellular diazotrophic cyanobacterium Crocosphaera contributes significantly to fixed nitrogen inputs in the oligotrophic ocean. In the western tropical South Pacific Ocean (WTSP), these diazotrophs abound thanks to the phosphorus-rich waters provided by the South Equatorial Current, and iron provided aeolian and subsurface volcanic activity. East of the WTSP, the South Pacific Gyre (SPG) harbors the most oligotrophic and transparent waters of the world's oceans, where only heterotrophic diazotrophs have been reported before. Here, in the SPG, we detected unexpected accumulation of Crocosphaera at 50 m with peak abundances of 5.26 × 105 nifH gene copies l–1. The abundance of Crocosphaera at 50 m was in the same order of magnitude as those detected westwards in the WTSP and represented 100% of volumetric N2 fixation rates. This accumulation at 50 m was likely due to a deeper penetration of UV light in the clear waters of the SPG being detrimental for Crocosphaera growth and N2 fixation activity. Nutrient and trace metal addition experiments did not induce any significant changes in N2 fixation or Crocosphaera abundance, indicating that this population was not limited by the resources tested and could develop in high numbers despite the oligotrophic conditions. Our findings indicate that the distribution of Crocosphaera can extend into subtropical gyres and further understanding of their controlling factors is needed. 

  • 2. Bonnet, Sophie
    et al.
    Caffin, Mathieu
    Berthelot, Hugo
    Grosso, Olivier
    Benavides, Mar
    Helias-Nunige, Sandra
    Guieu, Cecile
    Stenegren, Marcus
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    In-depth characterization of diazotroph activity across the western tropical South Pacific hotspot of N-2 fixation (OUTPACE cruise)2018In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 15, no 13, p. 4215-4232Article in journal (Refereed)
    Abstract [en]

    Here we report N-2 fixation rates from a similar to 4000 km transect in the western and central tropical South Pacific, a particularly undersampled region in the world ocean. Water samples were collected in the euphotic layer along a west to east transect from 160 degrees E to 160 degrees W that covered contrasting trophic regimes, from oligotrophy in the Melanesian archipelago (MA) waters to ultraoligotrophy in the South Pacific Gyre (GY) waters. N-2 fixation was detected at all 17 sampled stations with an average depth-integrated rate of 631 +/- 286 mu mol Nm(-2) d(-1) (range 196-1153 mu mol Nm(-2) d(-1)) in MA waters and of 85 +/- 79 mu mol Nm(-2) d(-1) (range 18-172 mu mol Nm(-2) d(-1)) in GY waters. Two cyanobacteria, the larger colonial filamentous Trichodesmium and the smaller UCYN-B, dominated the enumerated diazotroph community (>80 %) and gene expression of the nifH gene (cDNA > 10(5) nifH copies L-1) in MA waters. Single-cell isotopic analyses performed by nanoscale secondary ion mass spectrometry (nanoSIMS) at selected stations revealed that Trichodesmium was always the major contributor to N-2 fixation in MA waters, accounting for 47.1-83.8% of bulk N-2 fixation. The most plausible environmental factors explaining such exceptionally high rates of N-2 fixation in MA waters are discussed in detail, emphasizing the role of macro- and micro-nutrient (e.g., iron) availability, seawater temperature and currents.

  • 3. Caffin, Mathieu
    et al.
    Moutin, Thierry
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bouruet-Aubertot, Pascale
    Doglioli, Andrea Michelangelo
    Berthelot, Hugo
    Guieu, Cecile
    Grosso, Olivier
    Helias-Nunige, Sandra
    Leblond, Nathalie
    Gimenez, Audrey
    Petrenko, Anne Alexandra
    de Verneil, Alain
    Bonnet, Sophie
    N-2 fixation as a dominant new N source in the western tropical South Pacific Ocean (OUTPACE cruise)2018In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 15, no 8, p. 2565-2585Article in journal (Refereed)
    Abstract [en]

    We performed nitrogen (N) budgets in the photic layer of three contrasting stations representing different trophic conditions in the western tropical South Pacific (WTSP) Ocean during austral summer conditions (FebruaryMarch 2015). Using a Lagrangian strategy, we sampled the same water mass for the entire duration of each long-duration (5 days) station, allowing us to consider only vertical exchanges for the budgets. We quantified all major vertical N fluxes both entering (N-2 fixation, nitrate turbulent diffusion, atmospheric deposition) and leaving the photic layer (particulate N export). The three stations were characterized by a strong nitracline and contrasted deep chlorophyll maximum depths, which were lower in the oligotrophic Melanesian archipelago (MA, stations LD A and LD B) than in the ultra-oligotrophic waters of the South Pacific Gyre (SPG, station LD C). N-2 fixation rates were extremely high at both LD A (593 +/- 51 mu mol N m(-2) d(-1)) and LD B (706 +/- 302 mu mol N m(-2)d(-1)), and the diazotroph community was dominated by Trichodesmium. N-2 fixation rates were lower (59 +/- 16 mu mol N m(-2) d(-1)) at LD C, and the diazotroph community was dominated by unicellular N-2-fixing cyanobacteria (UCYN). At all stations, N-2 fixation was the major source of new N (> 90 %) before atmospheric deposition and upward nitrate fluxes induced by turbulence. N-2 fixation contributed circa 1318 % of primary production in the MA region and 3 in the SPG water and sustained nearly all new primary production at all stations. The e ratio (e ratio articulate carbon export / primary production) was maximum at LD A (9.7 ) and was higher than the e ratio in most studied oligotrophic regions (< 5), indicating a high efficiency of the WTSP to export carbon relative to primary production. The direct export of diazotrophs assessed by qPCR of the nifH gene in sediment traps represented up to 30.6 of the PC export at LD A, while their contribution was 5 and < 0.1 % at LD B and LD C, respectively. At the three studied stations, the sum of all N input to the photic layer exceeded the N output through organic matter export. This disequilibrium leading to N accumulation in the upper layer appears as a characteristic of the WTSP during the summer season.

  • 4.
    Caputo, Andrea
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Nylander, Johan A. A.
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration2019In: FEMS Microbiology Letters, ISSN 0378-1097, E-ISSN 1574-6968, Vol. 366, no 2, article id fny297Article in journal (Refereed)
    Abstract [en]

    Diatom diazotroph associations (DDAs) are a widespread marine planktonic symbiosis between several diatom genera and di-nitrogen (N2)-fixing bacteria. Combining single cell confocal microscopy observations and molecular genetic approaches on individual field collected cells, we determined the phylogenetic diversity, distribution and evolution of the DDAs. Confocal analyses coupled with 3-D imaging re-evaluated the cellular location of DDA symbionts. DDA diversity was resolved by paired gene sequencing (18S rRNA and rbcL genes, 16S rRNA and nifH genes). A survey using the newly acquired sequences against public databases found sequences with high similarity (99–100%) to either host (18S rRNA) or symbiont (16S rRNA) in atypical regions for DDAs (high latitudes, anoxic basin and copepod gut). Concatenated phylogenies were congruent for the host and cyanobacteria sequences and implied co-evolution. Time-calibrated trees dated the appearance of N2 fixing planktonic symbiosis from 100–50Mya and were consistent with the symbiont cellular location: symbioses with internal partners are more ancient. An ancestral state reconstruction traced the evolution of traits in DDAs and highlight that the adaptive radiation to the marine environment was likely facilitated by the symbiosis. Our results present the evolutionary nature of DDAs and provide new genetic and phenotypic information for these biogeochemically relevant populations.

  • 5.
    Caputo, Andrea
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Steiger, Miriam
    Pernice, Massimo Ciro
    Stenegren, Marcus
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Montoya, Joseph P.
    Subramaniam, Ajit
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Asymbiotic host and symbionts in a widely distributed N2 fixing planktonic symbiosis determined by new CARD-FISH assaysManuscript (preprint) (Other academic)
  • 6.
    Caputo, Andrea
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Stenegren, Marcus
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pernice, Massimo C.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    A short comparison of two marine planktonic diazotrophic symbioses highlights an un-quantified disparity2018In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 5, article id 2Article in journal (Refereed)
    Abstract [en]

    Some N2-fixing cyanobacteria form symbiosis with diverse protists. In the plankton two groups of diazotrophic symbioses are described: (1) a collective group of diatoms which associate with heterocystous cyanobacteria (Diatom Diazotroph Associations, DDA), and (2) the microalgal prymnesiophyte Braarudosphaera bigelowii and its relatives which associate with the unicellular cyanobacterium Candidatus Atelocyanobacterium thalassa (hereafter as UCYN-A). Both symbiotic systems co-occur, and in both partnerships the symbionts function as a nitrogen (N) source. In this perspective, we provide a brief comparison between the DDAs and the prymnesiophyte-UCYN-A symbioses highlighting similarities and differences in both systems, and present a bias in the attention and current methodology that has led to an under-detection and under-estimation of the DDAs.

  • 7. Cardini, Ulisse
    et al.
    Bednarz, Vanessa N.
    Naumann, Malik S.
    van Hoytema, Nanne
    Rix, Laura
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Al-Rshaidat, Mamoon M. D.
    Wild, Christian
    Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions2015In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, no 1818, article id 20152257Article in journal (Refereed)
    Abstract [en]

    Functional traits define species by their ecological role in the ecosystem. Animals themselves are host-microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N-2)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N-2 fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N-2 fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N-2 fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.

  • 8. Cardini, Ulisse
    et al.
    van Hoytema, Nanne
    Bednarz, Vanessa N.
    Rix, Laura
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Al-Rshaidat, Mamoon M. D.
    Wild, Christian
    Microbial dinitrogen fixation in coral holobionts exposed to thermal stress and bleaching2016In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 18, no 8, p. 2620-2633Article in journal (Refereed)
    Abstract [en]

    Coral holobionts (i.e., coral-algal-prokaryote symbioses) exhibit dissimilar thermal sensitivities that may determine which coral species will adapt to global warming. Nonetheless, studies simultaneously investigating the effects of warming on all holobiont members are lacking. Here we show that exposure to increased temperature affects key physiological traits of all members (herein: animal host, zooxanthellae and diazotrophs) of both Stylophora pistillata and Acropora hemprichii during and after thermal stress. S. pistillata experienced severe loss of zooxanthellae (i.e., bleaching) with no net photosynthesis at the end of the experiment. Conversely, A. hemprichii was more resilient to thermal stress. Exposure to increased temperature (+ 6 degrees C) resulted in a drastic increase in daylight dinitrogen (N-2) fixation, particularly in A. hemprichii (threefold compared with controls). After the temperature was reduced again to in situ levels, diazotrophs exhibited a reversed diel pattern of activity, with increased N-2 fixation rates recorded only in the dark, particularly in bleached S. pistillata (twofold compared to controls). Concurrently, both animal hosts, but particularly bleached S. pistillata, reduced both organic matter release and heterotrophic feeding on picoplankton. Our findings indicate that physiological plasticity by coral-associated diazotrophs may play an important role in determining the response of coral holobionts to ocean warming.

  • 9. Conroy, Brandon J.
    et al.
    Steinberg, Deborah K.
    Song, Bongkuen
    Kalmbach, Andrew
    Carpenter, Edward J.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. University of California, United States.
    Mesozooplankton Graze on Cyanobacteria in the Amazon River Plume and Western Tropical North Atlantic2017In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 8, article id 1436Article in journal (Refereed)
    Abstract [en]

    Diazotrophic cyanobacteria, those capable of fixing di-nitrogen (N2), are considered one of the major sources of new nitrogen (N) in the oligotrophic tropical ocean, but direct incorporation of diazotrophic N into food webs has not been fully examined. In the Amazon River-influenced western tropical North Atlantic (WTNA), diatom diazotroph associations (DDAs) and the filamentous colonial diazotrophs Trichodesmium have seasonally high abundances. We sampled epipelagic mesozooplankton in the Amazon River plume and WTNA in May-June 2010 to investigate direct grazing by mesozooplankton on two DDA populations: Richelia associated with Rhizosolenia diatoms (het-1) and Hemiaulus diatoms (het-2), and on Trichodesmium using highly specific qPCR assays targeting nitrogenase genes (nifH). Both DDAs and Trichodesmium occurred in zooplankton gut contents, with higher detection of het-2 predominantly in calanoid copepods (2.33-16.76 nifH copies organism 1). Abundance of Trichodesmium was low (2.21-4.03 nifH copies organism 1), but they were consistently detected at high salinity stations (> 35) in calanoid copepods. This suggests direct grazing on DDAs, Trichodesmium filaments and colonies, or consumption as part of sinking aggregates, is common. In parallel with the qPCR approach, a next generation sequencing analysis of 16S rRNA genes identified that cyanobacterial assemblage associated with zooplankton guts was dominated by the non-diazotrophic unicellular phylotypes Synechococcus (56%) and Prochlorococcus (26%). However, in two separate calanoid copepod samples, two unicellular diazotrophs Candidatus Atelocyanobacterium thalassa (UCYN-A) and Crocosphaera watsonii (UCYN-B) were present, respectively, as a small component of cyanobacterial assemblages (< 2%). This study represents the first evidence of consumption of DDAs, Trichodesmium, and unicellular cyanobacteria by calanoid copepods in an area of the WTNA known for high carbon export. These diazotroph populations are quantitatively important in the global N budget, widespread and hence, the next step is to accurately quantify grazing. Nonetheless, these results highlight a direct pathway of diazotrophic N into the food web and have important implications for biogeochemical cycles, particularly oligotrophic regions where N-2 fixation is the main source of new nitrogen.

  • 10. Delmont, T. O.
    et al.
    Pierella Karlusich, J. J.
    Veseli, I.
    Fuessel, J.
    Eren, A. M.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bowler, C.
    Wincker, P.
    Pelletier, E.
    Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean2022In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 16, no 4, p. 927-936Article in journal (Refereed)
    Abstract [en]

    Biological nitrogen fixation contributes significantly to marine primary productivity. The current view depicts few cyanobacterial diazotrophs as the main marine nitrogen fixers. Here, we used 891 Tara Oceans metagenomes derived from surface waters of five oceans and two seas to generate a manually curated genomic database corresponding to free-living, filamentous, colony-forming, particle-attached, and symbiotic bacterial and archaeal populations. The database provides the genomic content of eight cyanobacterial diazotrophs including a newly discovered population related to known heterocystous symbionts of diatoms, as well as 40 heterotrophic bacterial diazotrophs that considerably expand the known diversity of abundant marine nitrogen fixers. These 48 populations encapsulate 92% of metagenomic signal for known nifH genes in the sunlit ocean, suggesting that the genomic characterization of the most abundant marine diazotrophs may be nearing completion. Newly identified heterotrophic bacterial diazotrophs are widespread, express their nifH genes in situ, and also occur in large planktonic size fractions where they might form aggregates that provide the low-oxygen microenvironments required for nitrogen fixation. Critically, we found heterotrophic bacterial diazotrophs to be more abundant than cyanobacterial diazotrophs in most metagenomes from the open oceans and seas, emphasizing the importance of a wide range of heterotrophic populations in the marine nitrogen balance.

  • 11. Flores, Enrique
    et al.
    Romanovicz, Dwight K.
    Nieves-Moríon, Mercedes
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Villareal, Tracy A.
    Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom2022In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 13, article id 799362Article in journal (Refereed)
    Abstract [en]

    The symbiosis between the diatom Hemiaulus hauckii and the heterocyst-forming cyanobacterium Richelia intracellularis makes an important contribution to new production in the world’s oceans, but its study is limited by short-term survival in the laboratory. In this symbiosis, R. intracellularis fixes atmospheric dinitrogen in the heterocyst and provides H. hauckii with fixed nitrogen. Here, we conducted an electron microscopy study of H. hauckii and found that the filaments of the R. intracellularis symbiont, typically composed of one terminal heterocyst and three or four vegetative cells, are located in the diatom’s cytoplasm not enclosed by a host membrane. A second prokaryotic cell was also detected in the cytoplasm of H. hauckii, but observations were infrequent. The heterocysts of R. intracellularis differ from those of free-living heterocyst-forming cyanobacteria in that the specific components of the heterocyst envelope seem to be located in the periplasmic space instead of outside the outer membrane. This specialized arrangement of the heterocyst envelope and a possible association of the cyanobacterium with oxygen-respiring mitochondria may be important for protection of the nitrogen-fixing enzyme, nitrogenase, from photosynthetically produced oxygen. The cell envelope of the vegetative cells of R. intracellularis contained numerous membrane vesicles that resemble the outer-inner membrane vesicles of Gram-negative bacteria. These vesicles can export cytoplasmic material from the bacterial cell and, therefore, may represent a vehicle for transfer of fixed nitrogen from R. intracellularis to the diatom’s cytoplasm. The specific morphological features of R. intracellularis described here, together with its known streamlined genome, likely represent specific adaptations of this cyanobacterium to an intracellular lifestyle.

  • 12.
    Foster, Rachel A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Zehr, Jonathan P.
    Diversity, Genomics, and Distribution of Phytoplankton- Cyanobacterium Single-Cell Symbiotic Associations2019In: Annual Review of Microbiology, ISSN 0066-4227, E-ISSN 1545-3251, Vol. 73, p. 435-456Article, review/survey (Refereed)
    Abstract [en]

    Cyanobacteria are common in symbiotic relationships with diverse multicellular organisms (animals, plants, fungi) in terrestrial environments and with single-celled heterotrophic, mixotrophic, and autotrophic protists in aquatic environments. In the sunlit zones of aquatic environments, diverse cyanobacterial symbioses exist with autotrophic taxa in phytoplankton, including dinoflagellates, diatoms, and haptophytes (prymnesiophytes). Phototrophic unicellular cyanobacteria related to Synechococcus and Prochlorococcus are associated with a number of groups. N-2-fixing cyanobacteria are symbiotic with diatoms and haptophytes. Extensive genome reduction is involved in the N-2-fixing endosymbionts, most dramatically in the unicellular cyanobacteria associated with haptophytes, which have lost most of the photosynthetic apparatus, the ability to fix C, and the tricarboxylic acid cycle. The mechanisms involved in N-2-fixing symbioses may involve more interactions beyond simple exchange of fixed C for N. N-2-fixing cyanobacterial symbioses are widespread in the oceans, even more widely distributed than the best-known free-living N-2-fixing cyanobacteria, suggesting they may be equally or more important in the global ocean biogeochemical cycle of N.

  • 13.
    Foster, Rachel Ann
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. University of California, USA; Max Planck Institute for Marine Microbiology, Germany.
    Tienken, Daniela
    Littmann, Sten
    Whitehouse, Martin J.
    Kuypers, Marcel M. M.
    White, Angelicque E.
    The rate and fate of N2 and C fixation by marine diatom-diazotroph symbioses2022In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 16, no 2, p. 477-487Article in journal (Refereed)
    Abstract [en]

    N2 fixation constitutes an important new nitrogen source in the open sea. One group of filamentous N2 fixing cyanobacteria (Richelia intracellularis, hereafter Richelia) form symbiosis with a few genera of diatoms. High rates of N2 fixation and carbon (C) fixation have been measured in the presence of diatom-Richelia symbioses. However, it is unknown how partners coordinate C fixation and how the symbiont sustains high rates of N2 fixation. Here, both the N2 and C fixation in wild diatom-Richelia populations are reported. Inhibitor experiments designed to inhibit host photosynthesis, resulted in lower estimated growth and depressed C and N2 fixation, suggesting that despite the symbionts ability to fix their own C, they must still rely on their respective hosts for C. Single cell analysis indicated that up to 22% of assimilated C in the symbiont is derived from the host, whereas 78–91% of the host N is supplied from their symbionts. A size-dependent relationship is identified where larger cells have higher N2 and C fixation, and only N2 fixation was light dependent. Using the single cell measures, the N-rich phycosphere surrounding these symbioses was estimated and contributes directly and rapidly to the surface ocean rather than the mesopelagic, even at high estimated sinking velocities (<10 m d−1). Several eco-physiological parameters necessary for incorporating symbiotic N2 fixing populations into larger basin scale biogeochemical models (i.e., N and C cycles) are provided.

  • 14.
    Gamba, Andrea
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Petras, Daniel
    Little, Mark
    White, Brandie
    Dorrestein, Pieter C.
    Rohwer, Forest
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Hartmann, Aaron C.
    Applying Tissue Separation and Untargeted Metabolomics to Understanding Lipid Saturation Kinetics of Host Mitochondria and Symbiotic Algae in Corals Under High Temperature Stress2022In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 9, article id 853554Article in journal (Refereed)
    Abstract [en]

    Untargeted metabolomics is a powerful tool for profiling the biochemical phenotypes of organisms and discovering new metabolites that drive biological function and might be exploited as pharmaceutical leads. Yet, connecting physiological processes to metabolites detected remains a challenge due to the lack of structural and activity annotations and the underlying complexity of mixed samples (e.g., multiple microorganisms, organelles, etc.). To simplify this biological complexity, we separated coral holobionts into host mitochondria and their algal symbionts prior to LC-MS/MS-based untargeted metabolomic analysis followed by molecular networking. We found distinct metabolomic profiles between tissue fractions. Notably, 14% of metabolites detected were only observed in the mitochondria and algal symbionts, not in the holobiont, and thus were masked when the bulk (holobiont) sample was analyzed. The utility of tissue separation for hypothesis testing was assessed using a simple temperature experiment. We tested the hypothesis that membrane lipids of the coral mitochondria and algal symbionts become more saturated at higher temperatures to maintain membrane rigidity. While the holobiont metabolite profiles showed little change in response to elevated temperature, there was a change in lipid saturation of both fractions through time. The fatty acid saturation of both the coral mitochondria and the algal symbionts shifted upon exposure to higher temperatures (1 h) then returned to ambient saturation levels by 4 h, indicating rapid acclimatization to warmer water. Surprisingly, the fractions deviated in opposite directions: during the first hour of the experiment, the mitochondria showed an increase in saturated lipid concentrations, while the algal symbionts showed an increase in unsaturated lipids. Partitioning the holobiont prior to untargeted metabolomic analysis revealed disparate responses to environmental stress that would have gone undetected if only the holobiont/bulk tissue was analyzed. This work illustrates rapid physiological acclimatization to environmental changes in specific host organelles and symbionts, though via different paths.

  • 15.
    Grujcic, Vesna
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Taylor, Gordon T.
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    One Cell at a Time: Advances in Single-Cell Methods and Instrumentation for Discovery in Aquatic Microbiology2022In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 13, article id 881018Article in journal (Refereed)
    Abstract [en]

    Studying microbes from a single-cell perspective has become a major theme and interest within the field of aquatic microbiology. One emerging trend is the unfailing observation of heterogeneity in activity levels within microbial populations. Wherever researchers have looked, intra-population variability in biochemical composition, growth rates, and responses to varying environmental conditions has been evident and probably reflect coexisting genetically distinct strains of the same species. Such observations of heterogeneity require a shift away from bulk analytical approaches and development of new methods or adaptation of existing techniques, many of which were first pioneered in other, unrelated fields, e.g., material, physical, and biomedical sciences. Many co-opted approaches were initially optimized using model organisms. In a field with so few cultivable models, method development has been challenging but has also contributed tremendous insights, breakthroughs, and stimulated curiosity. In this perspective, we present a subset of methods that have been effectively applied to study aquatic microbes at the single-cell level. Opportunities and challenges for innovation are also discussed. We suggest future directions for aquatic microbiological research that will benefit from open access to sophisticated instruments and highly interdisciplinary collaborations.

  • 16. Hunt, Brian P. V.
    et al.
    Bonnet, Sophie
    Berthelot, Hugo
    Conroy, Brandon J.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pagano, Marc
    Contribution and pathways of diazotroph-derived nitrogen to zooplankton during the VAHINE mesocosm experiment in the oligotrophic New Caledonia lagoon2016In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 13, no 10, p. 3131-3145Article in journal (Refereed)
    Abstract [en]

    In oligotrophic tropical and subtropical oceans, where strong stratification can limit the replenishment of surface nitrate, dinitrogen (N-2) fixation by diazotrophs can represent a significant source of nitrogen (N) for primary production. The VAHINE (VAriability of vertical and tropHIc transfer of fixed N-2 in the south-wEst Pacific) experiment was designed to examine the fate of diazotroph-derived nitrogen (DDN) in such ecosystems. In austral summer 2013, three large ( similar to aEuro parts per thousand aEuro-50aEuro-m(3)) in situ mesocosms were deployed for 23 days in the New Caledonia lagoon, an ecosystem that typifies the low-nutrient, low-chlorophyll environment, to stimulate diazotroph production. The zooplankton component of the study aimed to measure the incorporation of DDN into zooplankton biomass, and assess the role of direct diazotroph grazing by zooplankton as a DDN uptake pathway. Inside the mesocosms, the diatom-diazotroph association (DDA) het-1 predominated during days 5-15 while the unicellular diazotrophic cyanobacteria UCYN-C predominated during days 15-23. A Trichodesmium bloom was observed in the lagoon (outside the mesocosms) towards the end of the experiment. The zooplankton community was dominated by copepods (63aEuro-% of total abundance) for the duration of the experiment. Using two-source N isotope mixing models we estimated a mean similar to aEuro parts per thousand aEuro-28aEuro-% contribution of DDN to zooplankton nitrogen biomass at the start of the experiment, indicating that the natural summer peak of N-2 fixation in the lagoon was already contributing significantly to the zooplankton. Stimulation of N-2 fixation in the mesocosms corresponded with a generally low-level enhancement of DDN contribution to zooplankton nitrogen biomass, but with a peak of similar to aEuro parts per thousand aEuro-73aEuro-% in mesocosm 1 following the UCYN-C bloom. qPCR analysis targeting four of the common diazotroph groups present in the mesocosms (Trichodesmium, het-1, het-2, UCYN-C) demonstrated that all four were ingested by copepod grazers, and that their abundance in copepod stomachs generally corresponded with their in situ abundance. N-15(2) labelled grazing experiments therefore provided evidence for direct ingestion and assimilation of UCYN-C-derived N by the zooplankton, but not for het-1 and Trichodesmium, supporting an important role of secondary pathways of DDN to the zooplankton for the latter groups, i.e. DDN contributions to the dissolved N pool and uptake by nondiazotrophs. This study appears to provide the first evidence of direct UCYN-C grazing by zooplankton, and indicates that UCYN-C-derived N contributes significantly to the zooplankton food web in the New Caledonia lagoon through a combination of direct grazing and secondary pathways.

  • 17. Karlusich, Juan José Pierella
    et al.
    Lombard, Fabien
    Irisson, Jean-Olivier
    Bowler, Chris
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Coupling Imaging and Omics in Plankton Surveys: State-of-the-Art, Challenges, and Future Directions2022In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 9, article id 878803Article in journal (Refereed)
    Abstract [en]

    A major challenge in characterizing plankton communities is the collection, identification and quantification of samples in a time-efficient way. The classical manual microscopy counts are gradually being replaced by high throughput imaging and nucleic acid sequencing. DNA sequencing allows deep taxonomic resolution (including cryptic species) as well as high detection power (detecting rare species), while RNA provides insights on function and potential activity. However, these methods are affected by database limitations, PCR bias, and copy number variability across taxa. Recent developments in high-throughput imaging applied in situ or on collected samples (high-throughput microscopy, Underwater Vision Profiler, FlowCam, ZooScan, etc) has enabled a rapid enumeration of morphologically-distinguished plankton populations, estimates of biovolume/biomass, and provides additional valuable phenotypic information. Although machine learning classifiers generate encouraging results to classify marine plankton images in a time efficient way, there is still a need for large training datasets of manually annotated images. Here we provide workflow examples that couple nucleic acid sequencing with high-throughput imaging for a more complete and robust analysis of microbial communities. We also describe the publicly available and collaborative web application EcoTaxa, which offers tools for the rapid validation of plankton by specialists with the help of automatic recognition algorithms. Finally, we describe how the field is moving with citizen science programs, unmanned autonomous platforms with in situ sensors, and sequencing and digitalization of historical plankton samples.

  • 18. Laeverenz Schlogelhofer, Hannah
    et al.
    Peaudecerf, Francois J.
    Bunbury, Freddy
    Whitehouse, Martin J.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Smith, Alison G.
    Croze, Ottavio A.
    Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism2021In: PLOS ONE, E-ISSN 1932-6203, Vol. 16, no 5, article id e0251643Article in journal (Refereed)
    Abstract [en]

    Microbial communities are of considerable significance for biogeochemical processes, for the health of both animals and plants, and for biotechnological purposes. A key feature of microbial interactions is the exchange of nutrients between cells. Isotope labelling followed by analysis with secondary ion mass spectrometry (SIMS) can identify nutrient fluxes and heterogeneity of substrate utilisation on a single cell level. Here we present a novel approach that combines SIMS experiments with mechanistic modelling to reveal otherwise inaccessible nutrient kinetics. The method is applied to study the onset of a synthetic mutualistic partnership between a vitamin B-12-dependent mutant of the alga Chlamydomonas reinhardtii and the B-12-producing, heterotrophic bacterium Mesorhizobium japonicum, which is supported by algal photosynthesis. Results suggest that an initial pool of fixed carbon delays the onset of mutualistic cross-feeding; significantly, our approach allows the first quantification of this expected delay. Our method is widely applicable to other microbial systems, and will contribute to furthering a mechanistic understanding of microbial interactions.

  • 19.
    Nieves-Morión, Mercedes
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Flores, Enrique
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Predicting substrate exchange in marine diatom-heterocystous cyanobacteria symbioses2020In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 22, no 6, p. 2027-2052Article, review/survey (Refereed)
    Abstract [en]

    In the open ocean, some phytoplankton establish symbiosis with cyanobacteria. Some partnerships involve diatoms as hosts and heterocystous cyanobacteria as symbionts. Heterocysts are specialized cells for nitrogen fixation, and a function of the symbiotic cyanobacteria is to provide the host with nitrogen. However, both partners are photosynthetic and capable of carbon fixation, and the possible metabolites exchanged and mechanisms of transfer are poorly understood. The symbiont cellular location varies from internal to partial to fully external, and this is reflected in the symbiont genome size and content. In order to identify the membrane transporters potentially involved in metabolite exchange, we compare the draft genomes of three differently located symbionts with known transporters mainly from model free-living heterocystous cyanobacteria. The types and numbers of transporters are directly related to the symbiont cellular location: restricted in the endosymbionts and wider in the external symbiont. Three proposed models of metabolite exchange are suggested which take into account the type of transporters in the symbionts and the influence of their cellular location on the available nutrient pools. These models provide a basis for several hypotheses that given the importance of these symbioses in global N and C budgets, warrant future testing.

  • 20.
    Nieves-Morión, Mercedes
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Flores, Enrique
    Whitehouse, Martin J.
    Thomen, Aurélien
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Single-Cell Measurements of Fixation and Intercellular Exchange of C and N in the Filaments of the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 71202021In: mBio, ISSN 2161-2129, E-ISSN 2150-7511, Vol. 12, no 4, article id e01314-21Article in journal (Refereed)
    Abstract [en]

    Under diazotrophic conditions, the model filamentous, heterocystforming cyanobacterium Anabaena sp. strain PCC 7120 develops a metabolic strategy based on the physical separation of the processes of oxygenic photosynthesis, in vegetative cells, and N-2 fixation, in heterocysts. This strategy requires the exchange of carbon and nitrogen metabolites and their distribution along the filaments, which takes place through molecular diffusion via septal junctions involving FraCD proteins. Here, Anabaena was incubated in a time course (up to 20 h) with [C-13]bicarbonate and N-15(2) and analyzed by secondary ion mass spectrometry imaging (SIMS) (large-geometry SIMS [LG- SIMS] and NanoSIMS) to quantify C and N assimilation and distribution in the filaments. The C-13/C-12 and N-15/N-14 ratios measured in wild-type filaments showed a general increase with time. The enrichment was relatively homogeneous in vegetative cells along individual filaments, while it was reduced in heterocysts. Heterocysts, however, accumulated recently fixed N at their poles, in which the cyanophycin plug [multi-L-arginyl-poly(L-aspartic acid)] is located. In contrast to the rather homogeneous label found along stretches of vegetative cells, C-13/C-12 and N-15/N-14 ratios were significantly different between filaments both at the same and different time points, showing high variability in metabolic states. A fraC fraD mutant did not fix N-2, and the C-13/C-12 ratio was homogeneous along the filament, including the heterocyst in contrast to the wild type. Our results show the consumption of reduced C in the heterocysts associated with the fixation and export of fixed N and present an unpredicted heterogeneity of cellular metabolic activity in different filaments of an Anabaena culture under controlled conditions.

    IMPORTANCE Filamentous, heterocyst- forming cyanobacteria represent a paradigm of multicellularity in the prokaryotic world. Physiological studies at the cellular level in model organisms are crucial to understand metabolic activities and qualify specific aspects related to multicellularity. Here, we used stable isotopes (C-13 and N-15) coupled to LG-SIMS and NanoSIMS imaging to follow single-cell C and N-2 fixation and metabolic dynamics along the filaments in the model heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. Our results show a close relationship between C and N fixation and distribution in the filaments and indicate that wild-type filaments in a culture can exhibit a substantial variability of metabolic states. This illustrates how some novel properties can be appreciated by studying microbial cultures at the single-cell level.

  • 21. Pierella Karlusich, Juan José
    et al.
    Pelletier, Eric
    Lombard, Fabien
    Carsique, Madeline
    Dvorak, Etienne
    Colin, Sébastien
    Picheral, Marc
    Cornejo-Castillo, Francisco M.
    Acinas, Silvia G.
    Pepperkok, Rainer
    Karsenti, Eric
    de Vargas, Colomban
    Wincker, Patrick
    Bowler, Chris
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods2021In: Nature Communications, E-ISSN 2041-1723, Vol. 12, no 1, article id 4160Article in journal (Refereed)
    Abstract [en]

    Nitrogen fixation has a critical role in marine primary production, yet our understanding of marine nitrogen-fixers (diazotrophs) is hindered by limited observations. Here, we report a quantitative image analysis pipeline combined with mapping of molecular markers for mining >2,000,000 images and >1300 metagenomes from surface, deep chlorophyll maximum and mesopelagic seawater samples across 6 size fractions (<0.2-2000<mu>m). We use this approach to characterise the diversity, abundance, biovolume and distribution of symbiotic, colony-forming and particle-associated diazotrophs at a global scale. We show that imaging and PCR-free molecular data are congruent. Sequence reads indicate diazotrophs are detected from the ultrasmall bacterioplankton (<0.2<mu>m) to mesoplankton (180-2000 mu m) communities, while images predict numerous symbiotic and colony-forming diazotrophs (>20 mu m). Using imaging and molecular data, we estimate that polyploidy can substantially affect gene abundances of symbiotic versus colony-forming diazotrophs. Our results support the canonical view that larger diazotrophs (>10 mu m) dominate the tropical belts, while unicellular cyanobacterial and non-cyanobacterial diazotrophs are globally distributed in surface and mesopelagic layers. We describe co-occurring diazotrophic lineages of different lifestyles and identify high-density regions of diazotrophs in the global ocean. Overall, we provide an update of marine diazotroph biogeographical diversity and present a new bioimaging-bioinformatic workflow. Nitrogen fixation by diazotrophs is critical for marine primary production. Using Tara Oceans datasets, this study combines a quantitative image analysis pipeline with metagenomic mining to provide an improved global overview of diazotroph abundance, diversity and distribution.

  • 22. Shao, Zhibo
    et al.
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Faculty of Science, Department of Materials and Environmental Chemistry (MMK).
    Luo, Ya-Wei
    Global oceanic diazotroph database version 2 and elevated estimate of globaloceanic N2 fixation2023In: Earth System Science Data, ISSN 1866-3508, E-ISSN 1866-3516, Vol. 15, no 8, p. 3673-3709Article in journal (Refereed)
    Abstract [en]

    Marine diazotrophs convert dinitrogen (N-2) gas into bioavailable nitrogen (N), supporting life in the global ocean. In 2012, the first version of the global oceanic diazotroph database (version 1) was published. Here, we present an updated version of the database (version 2), significantly increasing the number of in situ diazotrophic measurements from 13 565 to 55 286. Data points for N-2 fixation rates, diazotrophic cell abundance, and nifH gene copy abundance have increased by 184 %, 86 %, and 809 %, respectively. Version 2 includes two new data sheets for the nifH gene copy abundance of non-cyanobacterial diazotrophs and cell-specific N2 fixation rates. The measurements of N-2 fixation rates approximately follow a log-normal distribution in both version 1 and version 2. However, version 2 considerably extends both the left and right tails of the distribution. Consequently, when estimating global oceanic N-2 fixation rates using the geometric means of different ocean basins, version 1 and version 2 yield similar rates (43-57 versus 45-63 TgNyr (-1); ranges based on one geometric standard error). In contrast, when using arithmetic means, version 2 suggests a significantly higher rate of 223 +/- 30 TgNyr (-1) (mean +/- standard error; same hereafter) compared to version 1 (74 +/- 7 TgNyr (-1)). Specifically, substantial rate increases are estimated for the South Pacific Ocean (88 +/- 23 versus 20 +/- 2 TgNyr 1), primarily driven by measurements in the southwestern subtropics, and for the North Atlantic Ocean (40 +/- 9 versus 10 +/- 2 TgNyr (-1)). Moreover, version 2 estimates the N-2 fixation rate in the Indian Ocean to be 35 +/- 14 TgNyr (-1), which could not be estimated using version 1 due to limited data availability. Furthermore, a comparison of N-2 fixation rates obtained through different measurement methods at the same months, locations, and depths reveals that the conventional N-15(2) bubble method yields lower rates in 69% cases compared to the new N-15(2) dissolution method. This updated version of the database can facilitate future studies in marine ecology and biogeochemistry. The database is stored at the Figshare repository (https://doi.org/10.6084/m9.figshare.21677687; Shao et al., 2022).

  • 23. Smith, H. J.
    et al.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Max Planck Institute for Marine Microbiology, Germany .
    McKnight, D. M.
    Lisle, J. T.
    Littmann, S.
    Kuypers, M. M. M.
    Foreman, C. M.
    Microbial formation of labile organic carbon in Antarctic glacial environments2017In: Nature Geoscience, ISSN 1752-0894, E-ISSN 1752-0908, Vol. 10, no 5, p. 356-359Article in journal (Refereed)
    Abstract [en]

    Roughly six petagrams of organic carbon are stored within ice worldwide. This organic carbon is thought to be of old age and highly bioavailable. Along with storage of ancient and new atmospherically deposited organic carbon, microorganisms may contribute substantially to the glacial organic carbon pool. Models of glacial microbial carbon cycling vary from net respiration to net carbon fixation. Supraglacial streams have not been considered in models although they are amongst the largest ecosystems on most glaciers and are inhabited by diverse microbial communities. Here we investigate the biogeochemical sequence of organic carbon production and uptake in an Antarctic supraglacial stream in the McMurdo Dry Valleys using nanometre-scale secondary ion mass spectrometry, fluorescence spectroscopy, stable isotope analysis and incubation experiments. We find that heterotrophic production relies on highly labile organic carbon freshly derived from photosynthetic bacteria rather than legacy organic carbon. Exudates from primary production were utilized by heterotrophs within 24 h, and supported bacterial growth demands. The tight coupling of microbially released organic carbon and rapid uptake by heterotrophs suggests a dynamic local carbon cycle. Moreover, as temperatures increase there is the potential for positive feedback between glacial melt and microbial transformations of organic carbon.

  • 24. Smith, Heidi J.
    et al.
    Schmit, Amber
    Foster, Rachel
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Max Planck Institute for Marine Microbiology, Germany.
    Littman, Sten
    Kuypers, Marcel M. M.
    Foreman, Christine M.
    Biofilms on glacial surfaces: hotspots for biological activity2016In: npj Biofilms and Microbiomes, E-ISSN 2055-5008, Vol. 2, article id UNSP 16008Article in journal (Refereed)
    Abstract [en]

    Glaciers are important constituents in the Earth's hydrological and carbon cycles, with predicted warming leading to increases in glacial melt and the transport of nutrients to adjacent and downstream aquatic ecosystems. Microbial activity on glacial surfaces has been linked to the biological darkening of cryoconite particles, affecting albedo and increased melt. This phenomenon, however, has only been demonstrated for alpine glaciers and the Greenland Ice Sheet, excluding Antarctica. In this study, we show via confocal laser scanning microscopy that microbial communities on glacial surfaces in Antarctica persist in biofilms. Overall, similar to 35% of the cryoconite sediment surfaces were covered by biofilm. Nanoscale scale secondary ion mass spectrometry measured significant enrichment of C-13 and N-15 above background in both Bacteroidetes and filamentous cyanobacteria (i.e., Oscillatoria) when incubated in the presence of C-13-NaHCO3 and (NH4)-N-15. This transfer of newly synthesised organic compounds was dependent on the distance of heterotrophic Bacteroidetes from filamentous Oscillatoria. We conclude that the spatial organisation within these biofilms promotes efficient transfer and cycling of nutrients. Further, these results support the hypothesis that biofilm formation leads to the accumulation of organic matter on cryoconite minerals, which could influence the surface albedo of glaciers.

  • 25. Spungin, Dina
    et al.
    Belkin, Natalia
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Stenegren, Marcus
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Caputo, Andrea
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pujo-Pay, Mireille
    Leblond, Nathalie
    Dupouy, Cecile
    Bonnet, Sophie
    Berman-Frank, Ilana
    Programmed cell death in diazotrophs and the fate of organic matter in the western tropical South Pacific Ocean during the OUTPACE cruise2018In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 15, no 12, p. 3893-3908Article in journal (Refereed)
    Abstract [en]

    The fate of diazotroph (N-2 fixers) derived carbon (C) and nitrogen (N) and their contribution to vertical export of C and N in the western tropical South Pacific Ocean was studied during OUTPACE (Oligotrophy to UlTra-oligotrophy PACific Experiment). Our specific objective during OUTPACE was to determine whether autocatalytic programmed cell death (PCD), occurring in some diazotrophs, is an important mechanism affecting diazotroph mortality and a factor regulating the vertical flux of organic matter and, thus, the fate of the blooms. We sampled at three long duration (LD) stations of 5 days each (LDA, LDB and LDC) where drifting sediment traps were deployed at 150, 325 and 500m depth. LDA and LDB were characterized by high chlorophyll a (Chl a) concentrations (0.2-0.6 mu g L-1) and dominated by dense biomass of the filamentous cyanobacterium Trichodesmium as well as UCYN-B and diatom-diazotroph associations (Rhizosolenia with Richelia-detected by microscopy and het-1 nifH copies). Station LDC was located at an ultra-oligotrophic area of the South Pacific gyre with extremely low Chl a concentration (similar to 0.02 mu g L-1) with limited biomass of diazotrophs predominantly the unicellular UCYN-B. Our measurements of biomass from LDA and LDB yielded high activities of caspase-like and metacaspase proteases that are indicative of PCD in Trichodesmium and other phytoplankton. Metacaspase activity, reported here for the first time from oceanic populations, was highest at the surface of both LDA and LDB, where we also obtained high concentrations of transparent exopolymeric particles (TEP). TEP were negatively correlated with dissolved inorganic phosphorus and positively coupled to both the dissolved and particulate organic carbon pools. Our results reflect the increase in TEP production under nutrient stress and its role as a source of sticky carbon facilitating aggregation and rapid vertical sinking. Evidence for bloom decline was observed at both LDA and LDB. However, the physiological status and rates of decline of the blooms differed between the stations, influencing the amount of accumulated diazotrophic organic matter and mass flux observed in the traps during our experimental time frame. At LDA sediment traps contained the greatest export of particulate matter and significant numbers of both intact and decaying Trichodesmium, UCYN-B and het-1 compared to LDB where the bloom decline began only 2 days prior to leaving the station and to LDC where no evidence for bloom or bloom decline was seen. Substantiating previous findings from laboratory cultures linking PCD to carbon export in Trichodesmium, our results from OUTPACE indicate that nutrient limitation may induce PCD in high biomass blooms such as displayed by Trichodesmium or diatom-diazotroph associations. Furthermore, PCD combined with high TEP production will tend to facilitate cellular aggregation and bloom termination and will expedite vertical flux to depth.

  • 26.
    Stenegren, Marcus
    et al.
    Stockholm University, Faculty of Science, Department of Materials and Environmental Chemistry (MMK).
    Berg, Carlo
    Padilla, Cory C.
    David, Stefan-Sebastian
    Montoya, Joseph P.
    Yager, Patricia L.
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Materials and Environmental Chemistry (MMK). Max Planck Institute for Marine Microbiology, Germany; University of California, USA.
    Piecewise structural equation model (SEM) disentangles the environmental conditions favoring diatom diazotroph associations (DDAs) in the western tropical North Atlantic (WTNA)2017In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 8, article id 810Article in journal (Refereed)
    Abstract [en]

    Diatom diazotroph associations (DDAs) are important components in the world's oceans, especially in the western tropical north Atlantic (WTNA), where blooms have a significant impact on carbon and nitrogen cycling. However, drivers of their abundances and distribution patterns remain unknown. Here, we examined abundance and distribution patterns for two DDA populations in relation to the Amazon River (AR) plume in the WTNA. Quantitative PCR assays, targeting two DDAs (het-1 and het-2) by their symbiont's nifH gene, served as input in a piecewise structural equation model (SEM). Collections were made during high (spring 2010) and low (fall 2011) flow discharges of the AR. The distributions of dissolved nutrients, chlorophyll-a, and DDAs showed coherent patterns indicative of areas influenced by the AR. A symbiotic Hemiaulus hauckii-Richelia (het-2) bloom (> 10(6) cells L-1) occurred during higher discharge of the AR and was coincident with mesohaline to oceanic (30-35) sea surface salinities (SSS), and regions devoid of dissolved inorganic nitrogen (DIN), low concentrations of both DIP (> 0.1 mu mol L-1) and Si (> 1.0 mu mol L-1). The Richelia (het-1) associated with Rhizosolenia was only present in 2010 and at lower densities (10-1.76 x 10(5) nifH copies L-1) than het-2 and limited to regions of oceanic SSS (> 36). The het-2 symbiont detected in 2011 was associated with H. membranaceus (> 10(3) nifH copies L-1) and were restricted to regions with mesohaline SSS (31.8-34.3), immeasurable DIN, moderate DIP (0.1-0.60 mu mol L-1) and higher Si (4.19-22.1 mu mol L-1). The piecewise SEM identified a profound direct negative effect of turbidity on the het-2 abundance in spring 2010, while DIP and water turbidity had a more positive influence in fall 2011, corroborating our observations of DDAs at subsurface maximas. We also found a striking difference in the influence of salinity on DDA symbionts suggesting a niche differentiation and preferences in oceanic and mesohaline salinities by het-1 and het-2, respectively. The use of the piecewise SEM to disentangle the complex and concomitant hydrography of the WTNA acting on two biogeochemically relevant populations was novel and underscores its use to predict conditions favoring abundance and distributions of microbial populations.

  • 27.
    Stenegren, Marcus
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Caputo, Andrea
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Berg, Carlo
    Bonnet, Sophie
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific2018In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 15, no 5, p. 1559-1578Article in journal (Refereed)
    Abstract [en]

    The abundance and distribution of cyanobacterial diazotrophs were quantified in two regions (Melanesian archipelago, MA; and subtropical gyre, SG) of the western tropical South Pacific using nifH quantitative polymerase chain reaction (qPCR) assays. UCYN-A1 and A2 host populations were quantified using 18S rRNA qPCR assays including one newly developed assay. All phylotypes were detected in the upper photic zone (0-50 m), with higher abundances in the MA region. Trichodesmium and UCYN-B dominated and ranged from 2.18 x 10(2) to 9.41 x 10(6) and 1.10 x 10(2) to 2.78 x 10(6) nifH copies L-1, respectively. Het-1 (symbiont of Rhizosolenia diatoms) was the next most abundant (1.40 x 10(1)-1.74 x 10(5) nifH copies L-1) and co-occurred with het-2 and het-3. UCYN-A1 and A2 were the least abundant diazotrophs and were below detection (bd) in 63 and 79, respectively, of 120 samples. In addition, in up to 39% of samples in which UCYN-A1 and A2 were detected, their respective hosts were bd. Pairwise comparisons of the nifH abundances and various environmental parameters supported two groups: a deep-dwelling group (45 m) comprised of UCYN-A1 and A2 and a surface group (0-15 m) comprised of Trichodesmium, het-1 and het-2. Temperature and photosynthetically active radiation were positively correlated with the surface group, while UCYN-A1 and A2 were positively correlated with depth, salinity, and oxygen. Similarly, in a meta-analysis of 11 external datasets, all diazotrophs, except UCYN-A were correlated with temperature. Combined, our results indicate that conditions favoring the UCYN-A symbiosis differ from those of diatom diazotroph associations and free-living cyanobacterial diazotrophs.

  • 28.
    Stenegren, Marcus
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Weber, Sarah C.
    Brodin, David
    Subramaniam, Ajit
    Montoya, Joseph P.
    Voss, Maren
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Insights on symbiotic diatom diazotroph associations in the South China Sea by targeted microarray analysis of three symbiont strainsManuscript (preprint) (Other academic)
    Abstract [en]

    Three heterocystous cyanobacterial strains (two Richelia intracellularis: RintHH01, RintRC01, Calothrix rhizosoleniae: CalSC01) are known to form highly specific, intimate associations with several lineages of diatoms. Collectively these symbioses are unique since the cellular location varies from internal, partially integrated, and fully external; hence the immediate environment of the symbiont differs. We investigated the environmental gene expression levels of the three strains using a targeted mRNA microarray comprised of 748 genes on environmental samples collected in the South China Sea. Approximately half of the total genes (47%, 354 of the 748 genes) were expressed above background. The most highly transcribed genes were involved in photosynthesis, N2 fixation and potassium homeostasis, and strain differences were identifiable. The most important environmental parameters on the symbiont gene expression levels were fluorescence, temperature and beam transmission. However, salinity and oxygen impacted gene expression levels of one symbiont strain, RintHH01 differently (positively), possibly due to its different cellular location. Our results suggest that differences in gene expression patterns and environmental conditions influence the three closely related symbiont strains, and are likely related to their cellular location in their respective host diatoms.

  • 29.
    Sørensen, Megan E. S.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Heinrich Heine University, Germany.
    Zlatogursky, Vasily V.
    Onuţ-Brännström, Ioana
    Walraven, Anne
    Foster, Rachel Ann
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Burki, Fabien
    A novel kleptoplastidic symbiosis revealed in the marine centrohelid Meringosphaera with evidence of genetic integration2023In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 33, no 17, p. 3571-3584, e1-e6Article in journal (Refereed)
    Abstract [en]

    Plastid symbioses between heterotrophic hosts and algae are widespread and abundant in surface oceans. They are critically important both for extant ecological systems and for understanding the evolution of plastids. Kleptoplastidy, where the plastids of prey are temporarily retained and continuously re-acquired, provides opportunities to study the transitional states of plastid establishment. Here, we investigated the poorly studied marine centrohelid Meringosphaera and its previously unidentified symbionts using culture-independent methods from environmental samples. Investigations of the 18S rDNA from single-cell assembled genomes (SAGs) revealed uncharacterized genetic diversity within Meringosphaera that likely represents multiple species. We found that Meringosphaera harbors plastids of Dictyochophyceae origin (stramenopiles), for which we recovered six full plastid genomes and found evidence of two distinct subgroups that are congruent with host identity. Environmental monitoring by qPCR and catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) revealed seasonal dynamics of both host and plastid. In particular, we did not detect the plastids for 6 months of the year, which, combined with the lack of plastids in some SAGs, suggests that the plastids are temporary and the relationship is kleptoplastidic. Importantly, we found evidence of genetic integration of the kleptoplasts as we identified host-encoded plastid-associated genes, with evolutionary origins likely from the plastid source as well as from other alga sources. This is only the second case where host-encoded kleptoplast-targeted genes have been predicted in an ancestrally plastid-lacking group. Our results provide evidence for gene transfers and protein re-targeting as relatively early events in the evolution of plastid symbioses.

  • 30. Zielinski, Brian L.
    et al.
    Allen, Andrew E.
    Carpenter, Edward J.
    Coles, Victoria J.
    Crump, Byron C.
    Doherty, Mary
    Foster, Rachel A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. University of California, USA.
    Goes, Joaquim I.
    Gomes, Helga R.
    Hood, Raleigh R.
    McCrow, John P.
    Montoya, Joseph P.
    Moustafa, Ahmed
    Satinsky, Brandon M.
    Sharma, Shalabh
    Smith, Christa B.
    Yager, Patricia L.
    Paul, John H.
    Patterns of Transcript Abundance of Eukaryotic Biogeochemically-Relevant Genes in the Amazon River Plume2016In: PLOS ONE, E-ISSN 1932-6203, Vol. 11, no 9, article id e0160929Article in journal (Refereed)
    Abstract [en]

    The Amazon River has the largest discharge of all rivers on Earth, and its complex plume system fuels a wide array of biogeochemical processes, across a large area of the western tropical North Atlantic. The plume thus stimulates microbial processes affecting carbon sequestration and nutrient cycles at a global scale. Chromosomal gene expression patterns of the 2.0 to 156 mu m size-fraction eukaryotic microbial community were investigated in the Amazon River Plume, generating a robust dataset (more than 100 million mRNA sequences) that depicts the metabolic capabilities and interactions among the eukaryotic microbes. Combining classical oceanographic field measurements with metatranscriptomics yielded characterization of the hydrographic conditions simultaneous with a quantification of transcriptional activity and identity of the community. We highlight the patterns of eukaryotic gene expression for 31 biogeochemically significant gene targets hypothesized to be valuable within forecasting models. An advantage to this targeted approach is that the database of reference sequences used to identify the target genes was selectively constructed and highly curated optimizing taxonomic coverage, throughput, and the accuracy of annotations. A coastal diatom bloom highly expressed nitrate transporters and carbonic anhydrase presumably to support high growth rates and enhance uptake of low levels of dissolved nitrate and CO2. Diatom-diazotroph association (DDA: diatoms with nitrogen fixing symbionts) blooms were common when surface salinity was mesohaline and dissolved nitrate concentrations were below detection, and hence did not show evidence of nitrate utilization, suggesting they relied on ammonium transporters to aquire recently fixed nitrogen. These DDA blooms in the outer plume had rapid turnover of the photosystem D1 protein presumably caused by photodegradation under increased light penetration in clearer waters, and increased expression of silicon transporters as silicon became limiting. Expression of these genes, including carbonic anhydrase and transporters for nitrate and phosphate, were found to reflect the physiological status and biogeochemistry of river plume environments. These relatively stable patterns of eukaryotic transcript abundance occurred over modest spatiotemporal scales, with similarity observed in sample duplicates collected up to 2.45 km in space and 120 minutes in time. These results confirm the use of metatranscriptomics as a valuable tool to understand and predict microbial community function.

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