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Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column.

ABSTRACT: Ecological factors contributing to depth-related diversification of marine Thaumarchaeota populations remain largely unresolved. To investigate the role of potential microbial associations in shaping thaumarchaeal ecotype diversification, we examined co-occurrence relationships in a community composition dataset (16S rRNA V4-V5 region) collected as part of a 2-year time series in coastal Monterey Bay. Ecotype groups previously defined based on functional gene diversity-water column A (WCA), water column B (WCB) and Nitrosopumilus-like clusters-were recovered in the thaumarchaeal 16S rRNA gene phylogeny. Networks systematically reflected depth-related patterns in the abundances of ecotype populations, suggesting thaumarchaeal ecotypes as keystone members of the microbial community below the euphotic zone. Differential environmental controls on the ecotype populations were further evident in subnetwork modules showing preferential co-occurrence of OTUs belonging to the same ecotype cluster. Correlated abundances of Thaumarchaeota and heterotrophic bacteria (e.g., Bacteroidetes, Marinimicrobia and Gammaproteobacteria) indicated potential reciprocal interactions via dissolved organic matter transformations. Notably, the networks recovered ecotype-specific associations between thaumarchaeal and Nitrospina OTUs. Even at depths where WCB-like Thaumarchaeota dominated, Nitrospina OTUs were found to preferentially co-occur with WCA-like and Nitrosopumilus-like thaumarchaeal OTUs, highlighting the need to investigate the ecological implications of the composition of nitrifier assemblages in marine waters.

SUBMITTER: Reji L

PROVIDER: S-EPMC6474218 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column.

Reji Linta L Tolar Bradley B BB Smith Jason M JM Chavez Francisco P FP Francis Christopher A CA

The ISME journal 20190104 5

Ecological factors contributing to depth-related diversification of marine Thaumarchaeota populations remain largely unresolved. To investigate the role of potential microbial associations in shaping thaumarchaeal ecotype diversification, we examined co-occurrence relationships in a community composition dataset (16S rRNA V4-V5 region) collected as part of a 2-year time series in coastal Monterey Bay. Ecotype groups previously defined based on functional gene diversity-water column A (WCA), wate ...[more]

PMID: 30610232

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Project description:We sampled Thaumarchaeota populations in the northern Gulf of Mexico, including shelf waters under the Mississippi River outflow plume that are subject to recurrent hypoxia. Data from this study allowed us to: (1) test the hypothesis that Thaumarchaeota would be abundant in this region; (2) assess phylogenetic composition of these populations for comparison with other regions; (3) compare the efficacy of quantitative PCR (qPCR) based on primers for 16S rRNA genes (rrs) with primers for genes in the ammonia oxidation (amoA) and carbon fixation (accA, hcd) pathways; (4) compare distributions obtained by qPCR with the relative abundance of Thaumarchaeota rrs in pyrosequenced libraries; (5) compare Thaumarchaeota distributions with environmental variables to help us elucidate the factors responsible for the distributions; (6) compare the distribution of Thaumarchaeota with Nitrite-Oxidizing Bacteria (NOB) to gain insight into the coupling between ammonia and nitrite oxidation. We found up to 10(8)?copies?L(-1) of Thaumarchaeota rrs in our samples (up to 40% of prokaryotes) by qPCR, with maximum abundance in slope waters at 200-800?m. Thaumarchaeota rrs were also abundant in pyrosequenced libraries and their relative abundance correlated well with values determined by qPCR (r (2)?=?0.82). Thaumarchaeota populations were strongly stratified by depth. Canonical correspondence analysis using a suite of environmental variables explained 92% of the variance in qPCR-estimated gene abundances. Thaumarchaeota rrs abundance was correlated with salinity and depth, while accA abundance correlated with fluorescence and pH. Correlations of Archaeal amoA abundance with environmental variables were primer-dependent, suggesting differential responses of sub-populations to environmental variables. Bacterial amoA was at the limit of qPCR detection in most samples. NOB and Euryarchaeota rrs were found in the pyrosequenced libraries; NOB distribution was correlated with that of Thaumarchaeota (r (2)?=?0.49).

Project description:BackgroundThe ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here, we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore this, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S- and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans.ResultsWe found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts.ConclusionsThe differential action of ecological mechanisms seems to cause contrasting biogeography, in the tropical and subtropical ocean, among the smallest surface plankton, prokaryotes and picoeukaryotes. This suggests that the idiosyncrasy of the main constituents of the ocean microbiota should be considered in order to understand its current and future configuration, which is especially relevant in a context of global change, where the reaction of surface ocean plankton to temperature increase is still unclear. Video Abstract.

Dataset Information

Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column.

Publications

Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column.

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