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Genomic and morphological diversity of marine planktonic diatom-diazotroph associations: a continuum of integration and diversification through geological time
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Symbioses between eukaryotes and nitrogen (N2)-fixing cyanobacteria (or diazotrophs) are quite common in the plankton community. A few genera of diatoms (Bacillariophyceae) such as Rhizosolenia, Hemiaulus and Chaetoceros are well known to form symbioses with the heterocystous diazotrophic cyanobacteria Richelia intracellularis and Calothrix rhizosoleniae. The latter are also called diatom-diazotroph associations, or DDAs. Up to now, the prokaryotic partners have been morphologically and genetically characterized, and the phylogenetic reconstruction of the well conserved nifH gene (encodes for the nitrogenase enzyme) placed the symbionts in 3 clusters based on their host-specificity, i.e. het-1 (Rhizosolenia-R. intracellularis), het-2 (Hemiaulus-R. intracellularis), and het-3 (Chaetoceros-C- rhizosoleniae). Conversely, the diatom-hosts, major representative of the phytoplankton community and crucial contributors to the carbon (C) biogeochemical cycle, have been understudied.

The first aim of this thesis was to genetically and morphologically characterize the diatom-hosts, and to reconstruct the evolutionary background of the partnerships and the symbiont integration in the host. The molecular-clock analysis reconstruction showed the ancient appearance of the DDAs, and the traits characterizing the ancestors. In addition, diatom-hosts bearing internal symbionts (with more eroded draft genomes) appeared earlier than diatom-hosts with external symbionts. Finally a blast survey highlighted a broader distribution of the DDAs than expected.

The second aim of this thesis was to compare genetic and physiological characteristics of the DDAs symbionts with the other eukaryote-diazotroph symbiosis, i.e. prymnesiophyte-UCYN-A (or Candidatus Atelocyanobacterium thalassa). The genome comparison highlighted more genes for transporters in het-3 (external symbiont) and in the UCYN-A based symbiosis, suggesting that symbiont location might be relevant also for metabolic exchanges and interactions with the host and/or environment. Moreover, a summary of methodological biases that brought to an underestimation of the DDAs is reported.

The third aim of this thesis was to determine the distribution of the DDAs in the South Pacific Ocean using a quantitative polymerase chain reaction (qPCR) approach and to outline the environmental drivers of such distribution. Among the het-groups, het-1 was the most abundant/detected and co-occurred with the other 2 symbiotic strains, all responding similarly to the influence of abiotic factors, such as temperature and salinity (positive and negative correlation, respectively). Globally, Trichodesmium dominated the qPCR detections, followed by UCYN-B. UCYN-A phylotypes (A-1, A-2) were detected without their proposed hosts, for which new oligonucleotides were designed. The latter suggested a facultative symbiosis. Finally, microscopy observations of the het-groups highlighted a discrepancy with the qPCR counts (i.e. the former were several order of magnitudes lower), leading to the idea of developing a new approach to quantify the DDAs.  

The fourth aim of this thesis was to develop highly specific in situ hybridization assays (CARD-FISH) to determine the presence of alternative life-stages and/or free-living partners. The new assays were applied to samples collected in the South China Sea and compared with abundance estimates from qPCR assays for the 3 symbiotic strains. Free-living cells were indeed detected along the transect, mainly at deeper depths. Free-living symbionts had two morphotypes: trichomes and single-cells. The latter were interpreted as temporary life-stages. Consistent co-occurrence of the 3 het-groups was also found in the SCS and application of a SEM model predicted positive interactions between the het groups. We interpreted the positive interaction as absence of intra-specific competition, and consistent with the previous study, temperature and salinity were predicted as major drivers of the DDAs distribution.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2019. , p. 83
Keywords [en]
phytoplankton, diatoms, cyanobacteria, diazotrophs, symbiosis, evolution, phylogenetics, confocal microscopy, qPCR, CARD-FISH, tropics, sub-tropics
National Category
Biological Sciences Botany Ecology Evolutionary Biology Genetics Microbiology Oceanography, Hydrology and Water Resources
Research subject
Marine Ecology
Identifiers
URN: urn:nbn:se:su:diva-163027ISBN: 978-91-7797-556-4 (print)ISBN: 978-91-7797-557-1 (electronic)OAI: oai:DiVA.org:su-163027DiVA, id: diva2:1276419
Public defence
2019-02-22, P216. NPQ-huset, Svante Arrhenius väg 20, Stockholm, 09:30 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: In press. Paper 4: Manuscript.

Available from: 2019-01-30 Created: 2019-01-08 Last updated: 2019-01-22Bibliographically approved
List of papers
1. The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration
Open this publication in new window or tab >>The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration
2019 (English)In: FEMS Microbiology Letters, ISSN 0378-1097, E-ISSN 1574-6968Article in journal (Refereed) In press
Keywords
diatom, diazotroph, cyanobacteria, symbioses, evolution, distribution, confocal microscopy
National Category
Biological Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-163020 (URN)10.1093/femsle/fny297 (DOI)
Available from: 2018-12-11 Created: 2018-12-11 Last updated: 2019-01-08
2. 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: 2019-01-08Bibliographically approved
3. 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
Show others...
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: 2019-01-08Bibliographically approved
4. Asymbiotic host and symbionts in a widely distributed N2 fixing planktonic symbiosis determined by new CARD-FISH assays
Open this publication in new window or tab >>Asymbiotic host and symbionts in a widely distributed N2 fixing planktonic symbiosis determined by new CARD-FISH assays
Show others...
(English)Manuscript (preprint) (Other academic)
Keywords
DDAs, CARD-FISH, nifH, piecewise SEM, Mekong, diatoms, diazotrophs
National Category
Biological Sciences
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-163021 (URN)
Available from: 2018-12-11 Created: 2018-12-11 Last updated: 2019-01-08Bibliographically approved

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