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Functional and structural characterizations of phytoplankton-bacteria interactions in response to environmental challenges
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Marine Phytoplankton Ecology and Applications)ORCID iD: 0000-0002-8319-8766
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Microorganisms, such as phytoplankton and bacteria, make up ≈70% of aquatic biomass and contribute 50-85% of the oxygen in Earth’s atmosphere. The microbial loop concept and the discovery of the large diversity in microbial communities acknowledge that biotic interactions between microorganisms in addition to resource competition enable the recycling of energy and nutrients in aquatic food webs. In this thesis, I have studied interactions between phytoplankton and bacteria in three brackish systems of increasing complexity. Interactions were characterized in terms of structure and function, species-specificity aspects, influence on community resilience, and the link between interactions and cycling of energy and nutrients, using a combined approach of molecular techniques, morphology and biochemical analyses, and network analysis. Species-specific core microbiomes were identified in cultures of dinoflagellate isolates with varying genotypes or phenotypes, or from locations with varying levels of anthropogenic impact. We argue that the structure of phytoplankton-bacterial communities is influenced by predictable species-specific interactions, in addition to local abiotic conditions (such as salinity). When microalgal productivity exposed to seasonal variations in light and temperature was examined in photobioreactor polycultures, the stability of microalgal biomass linked to a high bacterial response diversity, primarily seen as shifts in taxonomy. When the structural and functional response of microalgae and bacteria to temperature shifts was coupled to resilience theories (adaptive cycles, panarchy and cross-scale resilience), results suggest that resilience was enabled through internal shifts in function and diversity within and across microalgal and bacterial levels, leading to maintenance of overall community function and diversity. Further, the results suggest that phytoplankton and bacteria in a coastal eutrophied location avoid competition for both energy and nutrients by resource partitioning, indicating that phytoplankton and bacteria might coexist more frequently in dynamic shallow coastal ecosystems than previously thought.

The results from this thesis emphasize the importance of considering community interactions between phytoplankton and bacteria when studying aquatic microbial communities, both in cultures and in complex field environments.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2020. , p. 260
Series
Linnaeus University Dissertations ; 390
Keywords [en]
Interactions, phytoplankton, microalgae, bacteria, communities, aquatic, diversity, functions, structure, species-specific, microbiome, core microbiome, response diversity, resilience, resource partitioning, competition, coexistence, amplicon sequencing, metatranscriptome
National Category
Environmental Sciences
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-97924Libris ID: drf4j9n7bmj89vz5ISBN: 978-91-89081-83-3 (print)ISBN: 978-91-89081-84-0 (electronic)OAI: oai:DiVA.org:lnu-97924DiVA, id: diva2:1463959
Public defence
2020-09-25, Fullriggaren, Ma135K, Pedalstråket 7, Kalmar, 14:00 (English)
Opponent
Supervisors
Available from: 2020-09-04 Created: 2020-09-03 Last updated: 2024-02-28Bibliographically approved
List of papers
1. Consistency in microbiomes in cultures of Alexandrium species isolated from brackish and marine waters
Open this publication in new window or tab >>Consistency in microbiomes in cultures of Alexandrium species isolated from brackish and marine waters
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2019 (English)In: Environmental Microbiology Reports, E-ISSN 1758-2229, Vol. 11, no 3, p. 425-433Article in journal (Refereed) Published
Abstract [en]

Phytoplankton and bacteria interactions have a significant role in aquatic ecosystem functioning. Associations can range from mutualistic to parasitic, shaping biogeochemical cycles and having a direct influence on phytoplankton growth. How variations in phenotype and sampling location, affect the phytoplankton microbiome is largely unknown. A high‐resolution characterization of the bacterial community in cultures of the dinoflagellate Alexandrium was performed on strains isolated from different geographical locations and at varying anthropogenic impact levels. Microbiomes of Baltic Sea Alexandrium ostenfeldii isolates were dominated by Betaproteobacteria and were consistent over phenotypic and genotypic Alexandrium strain variation, resulting in identification of an A. ostenfeldii core microbiome. Comparisons with in situ bacterial communities showed that taxa found in this A. ostenfeldii core were specifically associated to dinoflagellate dynamics in the Baltic Sea. Microbiomes of Alexandrium tamarense and minutum, isolated from the Mediterranean Sea, differed from those of A. ostenfeldii in bacterial diversity and composition but displayed high consistency, and a core set of bacterial taxa was identified. This indicates that Alexandrium isolates with diverse phenotypes host predictable, species‐specific, core microbiomes reflecting the abiotic conditions from which they were isolated. These findings enable in‐depth studies of potential interactions occurring between Alexandrium and specific bacterial taxa.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2019
Keywords
Algae, Bacteria, Interactions, Microbiome, Baltic Sea, Alexandrium, Alger, Bakterier, Interaktioner, Microbiom, Östersjön, Alexandrium
National Category
Ecology Microbiology
Research subject
Ecology, Microbiology; Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-81534 (URN)10.1111/1758-2229.12736 (DOI)000468000600014 ()30672139 (PubMedID)2-s2.0-85062772299 (Scopus ID)
Projects
EcoChange
Funder
Swedish Research Council FormasEU, European Research Council, 659453EU, Horizon 2020, 659453Carl Tryggers foundation , 14:283
Available from: 2019-04-01 Created: 2019-04-01 Last updated: 2024-07-04Bibliographically approved
2. Functional diversity facilitates resilience to environmental changes in long-term microalgal cultivation system
Open this publication in new window or tab >>Functional diversity facilitates resilience to environmental changes in long-term microalgal cultivation system
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(English)Manuscript (preprint) (Other academic)
National Category
Environmental Sciences
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-97926 (URN)
Available from: 2020-09-03 Created: 2020-09-03 Last updated: 2020-09-11Bibliographically approved
3. Temperature Stress Induces Shift From Co-Existence to Competition for Organic Carbon in Microalgae-Bacterial Photobioreactor Community – Enabling Continuous Production of Microalgal Biomass
Open this publication in new window or tab >>Temperature Stress Induces Shift From Co-Existence to Competition for Organic Carbon in Microalgae-Bacterial Photobioreactor Community – Enabling Continuous Production of Microalgal Biomass
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2021 (English)In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 12, no 11 February, p. 1-17, article id 607601Article in journal (Refereed) Published
Abstract [en]

To better predict the consequences of environmental change on aquatic microbial ecosystems it is important to understand what enables community resilience. The mechanisms by which a microbial community maintain its overall function, for example, the cycling of carbon, when exposed to a stressor, can be explored by considering three concepts: biotic interactions, functional adaptations, and community structure. Interactions between species are traditionally considered as, e.g., mutualistic, parasitic, or neutral but are here broadly defined as either coexistence or competition, while functions relate to their metabolism (e.g., autotrophy or heterotrophy) and roles in ecosystem functioning (e.g., oxygen production, organic matter degradation). The term structure here align with species richness and diversity, where a more diverse community is though to exhibit a broader functional capacity than a less diverse community. These concepts have here been combined with ecological theories commonly used in resilience studies, i.e., adaptive cycles, panarchy, and cross-scale resilience, that describe how the status and behavior at one trophic level impact that of surrounding levels. This allows us to explore the resilience of a marine microbial community, cultivated in an outdoor photobioreactor, when exposed to a naturally occurring seasonal stress. The culture was monitored for 6weeks during which it was exposed to two different temperature regimes (21 +/- 2 and 11 +/- 1 degrees C). Samples were taken for metatranscriptomic analysis, in order to assess the regulation of carbon uptake and utilization, and for amplicon (18S and 16S rRNA gene) sequencing, to characterize the community structure of both autotrophs (dominated by the green microalgae Mychonastes) and heterotrophs (associated bacterioplankton). Differential gene expression analyses suggested that community function at warm temperatures was based on concomitant utilization of inorganic and organic carbon assigned to autotrophs and heterotrophs, while at colder temperatures, the uptake of organic carbon was performed primarily by autotrophs. Upon the shift from high to low temperature, community interactions shifted from coexistence to competition for organic carbon. Network analysis indicated that the community structure showed opposite trends for autotrophs and heterotrophs in having either high or low diversity. Despite an abrupt change of temperature, the microbial community as a whole responded in a way that maintained the overall level of diversity and function within and across autotrophic and heterotrophic levels. This is in line with cross-scale resilience theory describing how ecosystems may balance functional overlaps within and functional redundancy between levels in order to be resilient to environmental change (such as temperature).

Place, publisher, year, edition, pages
Frontiers Media S.A., 2021
Keywords
microalgae; bacteria; community; resilience; coexistence; competition; adaptive cycles; interactions
National Category
Environmental Sciences
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-97927 (URN)10.3389/fmicb.2021.607601 (DOI)000621368600001 ()33643237 (PubMedID)2-s2.0-85101699588 (Scopus ID)
Available from: 2020-09-03 Created: 2020-09-03 Last updated: 2024-01-17Bibliographically approved
4. Resource partitioning between phytoplankton and bacteria in the coastal Baltic Sea
Open this publication in new window or tab >>Resource partitioning between phytoplankton and bacteria in the coastal Baltic Sea
(English)Manuscript (preprint) (Other academic)
National Category
Environmental Sciences
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-97928 (URN)
Available from: 2020-09-03 Created: 2020-09-03 Last updated: 2020-09-11Bibliographically approved

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