Disentangling the mechanisms shaping the surface ocean microbiota

Ramiro Logares,Josep M Gasol,Pedro C Junger,Silvia G Acinas,Anders K Krabberød,Carlos M Duarte,Clara Ruiz-González,Guillem Salazar,Ramon Massana,Laura Rubinat-Ripoll,Thomas S B Schmidt,Colomban De Vargas,Mireia Mestre,Ina M Deutschmann,Marta Sebastián,Caterina R Giner

doi:10.1186/s40168-020-00827-8

Abstract

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.8ZJi5SwgFNAgJoQiFLy3zUVideo

Highlights

The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences
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
Quantifying the mechanisms that structure the surface ocean picoplankton We analysed 16S and 18S rRNA-genes from prokaryotes and picoeukaryotes in 120 globally distributed tropical and subtropical stations sampled during the Malaspina 2010 expedition [30] (Fig. 1a; Figure S1, Additional file 1)

Summary

Introduction

The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. 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). We do not know whether these crucial components of the ocean microbiota are structured by the action of the same or different ecological processes Comprehending such processes is fundamental, as their differential action can produce changes in the ocean microbiota composition that could impact global ecosystem function [15,16,17]. A recent ecological synthesis explains the structure of communities and the emergence of biogeography as a consequence of the action of four main processes: selection, dispersal, ecological drift and speciation [18]. Speciation is the evolution of new species [18], and it will not be considered hereafter as it is expected to have a small impact in the turnover of communities that are connected via dispersal [23], being difficult to measure this ecological process in the wild

Methods

Results

Discussion

Conclusion