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Disentangling the Ecological Processes Shaping the Latitudinal Pattern of Phytoplankton Communities in the Pacific Ocean.

ABSTRACT: Phytoplankton diversity and community compositions vary across spaces and are fundamentally affected by several deterministic (e.g., environmental selection) and stochastic (e.g., ecological drift) processes. How this suite of different processes regulates the biogeography of phytoplankton remains to be comprehensively explored. Using high-throughput sequencing data and null model analysis, we revealed the ecological processes shaping the latitudinal community structure of three major phytoplankton groups (i.e., diatoms, Synechococcus, and haptophytes) across the Pacific Ocean (70°N, 170°W to 35°S, 170°W). At the basin scale, heterogeneous selection (selection under heterogeneous environmental conditions) dominated the assembly processes of all phytoplankton groups; however, its relative importance varied greatly at the climatic zonal scale, explaining the distinct latitudinal α- and β-diversity among phytoplankton groups. Assembly processes in Synechococcus and haptophyte communities were mainly controlled by physical and nutrient factors, respectively. High temperature drove Synechococcus communities to be more deterministic with higher diversity, while haptophyte communities were less environmentally selected at low latitudes due to their wide niche breadth and mixotrophic lifestyle. Diatom communities were overwhelmingly dominated by the selection process but with low correlation of measured environmental factors to their community compositions. This could be attributed to the high growth rate of diatoms, as indicated by their lower site occupation frequency than predicted in the neutral community model. Our study showed that heterogeneous selection is the main force that shaped the biogeography of three key phytoplankton groups in the Pacific Ocean, with a latitudinal variation of relative importance due to the distinct traits among phytoplankton. IMPORTANCE Phytoplankton are diverse and abundant as primary producers in the ocean, with diversity and community compositions varying spatially. How fundamental processes (e.g., selection, dispersal, and drift) regulate their global biogeography remains to be comprehensively explored. In this study, we disentangled the ecological processes of three key phytoplankton groups (i.e., diatoms, Synechococcus, and haptophytes) along the same latitudinal gradients in the Pacific Ocean. Heterogeneous selection, by promoting species richness and reducing similarity between communities, was the dominant process shaping the communities of each phytoplankton group at the basin scale. However, its relative importance varied greatly among different phytoplankton groups in different climate zones, explaining the uneven latitudinal α- and β-diversity. We also highlight the importance of identifying key factors mediating the relative importance of assembly processes in phytoplankton communities, which will enhance our understanding of their biogeography in the ocean and future patterns under climate changes.

SUBMITTER: Xu Z

PROVIDER: S-EPMC8725599 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Climate-change-induced alterations of oceanic conditions will lead to the ecological niches of some marine phytoplankton species disappearing, at least regionally. How will such losses affect the ecosystem and the coupled biogeochemical cycles? Here, we couch this question in terms of ecological redundancy (will other species be able to fill the ecological roles of the extinct species) and biogeochemical redundancy (can other species replace their biogeochemical roles). Prior laboratory and field studies point to a spectrum in the degree of redundancy. We use a global three-dimensional computer model with diverse planktonic communities to explore these questions further. The model includes 35 phytoplankton types that differ in size, biogeochemical function and trophic strategy. We run two series of experiments in which single phytoplankton types are either partially or fully eliminated. The niches of the targeted types were not completely reoccupied, often with a reduction in the transfer of matter from autotrophs to heterotrophs. Primary production was often decreased, but sometimes increased due to reduction in grazing pressure. Complex trophic interactions (such as a decrease in the stocks of a predator's grazer) led to unexpected reshuffling of the community structure. Alterations in resource utilization may cause impacts beyond the regions where the type went extinct. Our results suggest a lack of redundancy, especially in the 'knock on' effects on higher trophic levels. Redundancy appeared lowest for types on the edges of trait space (e.g. smallest) or with unique competitive strategies. Though highly idealized, our modelling findings suggest that the results from laboratory or field studies often do not adequately capture the ramifications of functional redundancy. The modelled, often counterintuitive, responses-via complex food web interactions and bottom-up versus top-down controls-indicate that changes in planktonic community will be key determinants of future ocean global change ecology and biogeochemistry.

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.

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Disentangling the Ecological Processes Shaping the Latitudinal Pattern of Phytoplankton Communities in the Pacific Ocean.

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