Disentangling the mechanisms shaping the surface ocean microbiota

Abstract

Background The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have largescale consequences. Yet, the underlaying 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 the previous, 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. Results We 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 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. Conclusions The 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.

Spatiotemporal dynamics of the archaeal community in coastal sediments: assembly process and co-occurrence relationship

“…Dispersal limitation accounted for~40% of the community variation across all samples. This proportion was higher than that reported for lake bacteria [26,77] and surface-ocean prokaryotes [78]. However, this is considered reasonable because sediment has a lower regional connectivity than water, which decreases the probability of active dispersal [66].…”

“…Homogeneous selection is one process in which environments constrain the divergence of microbial populations [28]. The prevalence of this process has also been found in lake bacterial (>70%) [26,77] and surfaceocean prokaryotic (~23-24% of the community variation) [78] communities. The indication is that several consistent environmental factors (e.g., the concentration (C/N) and source (δ 13 C) of organic matter that varied slightly across samples and/or unmeasured factors in this study) selected for similar microbial communities across samples.…”

“…Drift provided a lower explanatory power in the analysis based on the 99% cut-off than that based on the 97% cut-off, whereas an opposite trend was seen for dispersal limitation. OTUs clustered at different cut-offs may represent different taxonomic units with varying evolutionary rates, and thus may assemble under different mechanisms [78]. Additionally, the fluctuations may reflect the sensitivity of the null model analysis to the OTU number, in particular for the low-size archaeal population.…”

Decoding Populations in the Ocean Microbiome

“…Subsequent large-scale oceanographic campaigns, such as Malaspina [23], TARA Oceans [24], Bio-GO-SHIP [25], and GEOTRACES cruises [26], significantly expanded our comprehension of the magnitude of the ocean's microbiome diversity. These campaigns indicated ~50,000 -100,000 protists and ~10,000 -35,000 bacterial "species" or taxonomic units [16,27,28] in the open ocean plankton using High Throughput DNA Sequencing (HTS). From the metabolic-function perspective, TARA Oceans, based on sequencing microbial genome fragments (hereafter metagenomics), has cataloged ~47 million predominantly prokaryotic genes [29] and ~116 million eukaryotic genes [30] at the global-ocean plankton scale.…”

“…Even though the dispersal rate of most microbes is still unknown, indirect evidence points to high dispersal rates [52,54] that could be substantially higher than in multicellular organisms. Nevertheless, while it has been argued that organisms with <1mm of body size have virtually no barriers to dispersal [55], multiple studies during the last two decades point to dispersal limitation in microbes [28,52,54,56]. Furthermore, the reproductive rates of multicellular organisms tend to be lower than those of microbes.…”