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Significance of N2 fixing planktonic symbioses for open ocean ecosystems
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Di-nitrogen (N2) fixers, also called diazotrophs, are able to reduce atmospheric N2 into bioavailable nitrogen, giving them an advantage in open ocean regions with low dissolved inorganic nitrogen concentrations. The focus of this thesis are three lineages of symbiotic heterocystous filamentous types (het-1, het-2 and het-3), that associate with several genera of microalgae called diatoms (collectively referred to as Diatom Diazotroph Associations, DDAs). Other major cyanobacterial diazotrophs in the ocean are the filamentous Trichodesmium spp., and the unicellular UCYN-A, UCYN-B and UCYN-C. Although widespread in the tropics and subtropics, and first described in the early 20th century, the DDAs are an understudied group of diazotrophs. Hence, our knowledge of their distribution, abundance, activity, and how these are constrained by the environment is limited.

Initially we investigated the abundances and distributions of eight cyanobacterial diazotrophs, and two proposed micro-algal hosts of UCYN-A1 and A2, in the western tropical south Pacific (WTSP), using quantitative polymerase chain reaction (qPCR). Trichodesmium spp. was the most abundant diazotroph and het-1 was the most abundant DDA symbiont. Using correlation analysis a distinct vertical separation was observed between UCYN-A and the other diazotrophs (Trichodesmium spp., UCYN-B and DDA symbionts). The most influential environmental parameter on the diazotroph abundances in the WTSP was temperature, and in order to investigate this further we compiled qPCR data from 11 publicly available datasets from four ocean basins. Using a weighted meta-analysis we found that temperature was a robust factor governing the diazotroph abundances (except for UCYN-A) across ocean basins.

Attempting to identify differences in environmental impacts on two of the DDA symbiont strains (het-1 and het-2), we applied a new statistical tool called piecewise structural equation model, on qPCR abundance data from the western tropical North Atlantic. We saw that the two strains had a direct positive interaction between each other, but two parameters (salinity and dissolved inorganic phosphorous) differed. Based on a direct positive effect of salinity on het-1, and an indirect negative effect of salinity on het-2, we concluded that het-2 prefers intermediate salinities (30-35 PSU), which is consistent with where observations of het-2 blooms have been made.

Although DDA and UCYN-A symbionts both are major contributors of new N, and are symbiotic, they have several unique differences. The host partners differ in phylogeny (diatom vs prymnesiophyte), size (80-250 vs 7-10 µm) and the symbiotic life history (colonial vs solitary). The larger, colonial nature of DDAs make them difficult to collect, and hence they are often under-sampled and undetected. In fact, after reviewing 46 qPCR studies we found that < 30% of the studies (13 out of 46) quantified all three DDA symbionts, compared to UCYN-A (96%, 44 out of 46).

In order to study the DDA symbiont gene expressions we developed a highly specific DDA symbiont microarray (748 probes), which was applied on samples collected in the South China Sea. Although the gene expression levels were highly variable, we observed an upregulation of the nifH gene (for N2 fixation) in the night. Investigating environmental impact on overall gene expression levels, we found that fluorescence, temperature and salinity was most important. Temperature and salinity also constrained abundances, but fluorescence could be seen as a proxy for either other phytoplankton or light availability, suggesting that daylight and host influence DDA symbiont gene expression levels.

The results of this thesis broaden our understanding of the DDAs and how their ambient environment influences them. It has also opened up new possibilities for in depth analysis of these complex environmental impacts. Lastly, it has provided new analysis tools for further development on how the symbionts and hosts potentially impact each other’s activities.

Place, publisher, year, edition, pages
Stockholm: Department of ecology, environment and plant sciences, Stockholm University , 2020. , p. 105
Keywords [en]
nitrogen fixation, diazotrophs, symbiosis, DDA, cyanobacteria, qPCR, piecewise SEM, microarray, tropics, subtropics, marine, open ocean, Richelia, Calothrix
National Category
Ecology Microbiology
Research subject
Marine Ecology
Identifiers
URN: urn:nbn:se:su:diva-176275ISBN: 978-91-7797-933-3 (print)ISBN: 978-91-7797-934-0 (electronic)OAI: oai:DiVA.org:su-176275DiVA, id: diva2:1373556
Public defence
2020-01-10, Vivi Täckholmssalen, NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 4: Manuscript.

Available from: 2019-12-18 Created: 2019-11-27 Last updated: 2019-12-10Bibliographically approved
List of papers
1. Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific
Open this publication in new window or tab >>Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific
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2018 (English)In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 15, no 5, p. 1559-1578Article in journal (Refereed) Published
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.

National Category
Biological Sciences Earth and Related Environmental Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-154710 (URN)10.5194/bg-15-1559-2018 (DOI)000427515600003 ()
Available from: 2018-04-10 Created: 2018-04-10 Last updated: 2019-11-27Bibliographically approved
2. Piecewise structural equation model (SEM) disentangles the environmental conditions favoring diatom diazotroph associations (DDAs) in the western tropical North Atlantic (WTNA)
Open this publication in new window or tab >>Piecewise structural equation model (SEM) disentangles the environmental conditions favoring diatom diazotroph associations (DDAs) in the western tropical North Atlantic (WTNA)
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2017 (English)In: Frontiers in Microbiology, ISSN 1664-302X, E-ISSN 1664-302X, Vol. 8, article id 810Article in journal (Refereed) Published
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.

Keywords
symbioses, cyanobiont, diatoms, nifH, Amazon, DDAs, piecewise SEM
National Category
Biological Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-144843 (URN)10.3389/fmicb.2017.00810 (DOI)000401480300003 ()28536565 (PubMedID)
Available from: 2017-07-05 Created: 2017-07-05 Last updated: 2019-11-28Bibliographically approved
3. A short comparison of two marine planktonic diazotrophic symbioses highlights an un-quantified disparity
Open this publication in new window or tab >>A short comparison of two marine planktonic diazotrophic symbioses highlights an un-quantified disparity
2018 (English)In: Frontiers in Marine Science, E-ISSN 2296-7745, Vol. 5, article id 2Article in journal (Refereed) Published
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.

Keywords
cyanobacteria, diazotrophs, diatoms, symbiosis, DDA, UCYN-A, Richelia, Calothrix
National Category
Biological Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-162970 (URN)10.3389/fmars.2018.00002 (DOI)
Available from: 2018-12-10 Created: 2018-12-10 Last updated: 2019-11-27Bibliographically approved
4. Insights on symbiotic diatom diazotroph associations in the South China Sea by targeted microarray analysis of three symbiont strains
Open this publication in new window or tab >>Insights on symbiotic diatom diazotroph associations in the South China Sea by targeted microarray analysis of three symbiont strains
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(English)Manuscript (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.

Keywords
cyanobacteria, DDA, Richelia, Calothrix, symbiosis, gene expression, nitrogen fixation, nifH, microarray, Mekong River, South China Sea
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-174732 (URN)
Available from: 2019-11-27 Created: 2019-11-27 Last updated: 2019-12-03Bibliographically approved

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