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Disentangling the Mechanisms Shaping the Surface Ocean Microbiota Ramiro Logares1,2*, Ina M

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Disentangling the Mechanisms Shaping the Surface Ocean Microbiota Ramiro Logares1,2*, Ina M Logares et al. Microbiome (2020) 8:55 https://doi.org/10.1186/s40168-020-00827-8 RESEARCH Open Access Disentangling the mechanisms shaping the surface ocean microbiota Ramiro Logares1,2*, Ina M. Deutschmann1, Pedro C. Junger3, Caterina R. Giner1,4, Anders K. Krabberød2, Thomas S. B. Schmidt5, Laura Rubinat-Ripoll6, Mireia Mestre1,7,8, Guillem Salazar1,9, Clara Ruiz-González1, Marta Sebastián1,10, Colomban de Vargas6, Silvia G. Acinas1, Carlos M. Duarte11, Josep M. Gasol1,12 and Ramon Massana1 Abstract Background: The 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. 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, 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. (Continued on next page) * Correspondence: [email protected] 1Institute of Marine Sciences (ICM), CSIC, 08003 Barcelona, Catalonia, Spain 2Department of Biosciences, Section for Genetics and Evolutionary Biology, University of Oslo, 0316 Oslo, Norway Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Logares et al. Microbiome (2020) 8:55 Page 2 of 17 (Continued from previous page) 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. Keywords: Ocean, Plankton, Microbiota, Picoeukaryotes, Prokaryotes, Community structure, Ecological processes, Selection, Dispersal, Drift Background colonizers are too far away [20], and the significance of The surface ocean microbiota is a pivotal underpinning of dispersal limitation increases as geographic scale in- global biogeochemical cycles [1, 2]. The smallest ocean creases [21]. Ecological drift (hereafter drift) in a local microbes, the picoplankton, have a key role in the global community refers to random changes in species’ relative carbon cycle, being responsible for an important fraction abundances derived from stochastic birth, death, off- of the total atmospheric carbon and nitrogen fixation in spring production, immigration and emigration [18]. the ocean [3–5], which supports ≈ 46% of the global pri- The action of drift in a metacommunity, that is, local mary productivity [6]. Oceanic picoplankton plays a fun- communities that are connected via dispersal of multiple damental role in processing organic matter by recycling species [22], may lead to neutral dynamics [21], where nutrients and carbon to support additional production as random dispersal is the main mechanism of community well as by channelling organic carbon to upper trophic assembly. Finally, speciation is the evolution of new spe- levels through food webs [5, 7, 8]. The ocean picoplankton cies [18], and it will not be considered hereafter as it is includes prokaryotes (both bacteria and archaea) and tiny expected to have a small impact in the turnover of com- unicellular eukaryotes (hereafter picoeukaryotes), which munities that are connected via dispersal [23], being also feature fundamental differences in terms of cellular struc- difficult to measure this ecological process in the wild. ture, feeding habits, metabolic diversity, growth rates and The action of the previous ecological processes is typ- behaviour [9]. Even though marine picoeukaryotes and ically manifested as different taxonomic or phylogenetic prokaryotes are usually investigated separately, they are in- patterns of community turnover, that is, β-diversity. At timately connected through biogeochemical and food web the moment, there are several estimators of β-diversity networks [10–12]. which capture different aspects of community turnover The underlying ecological mechanisms determining [24]. Most of these indices consider taxonomic or phylo- the biogeography of prokaryotes and picoeukaryotes in genetic aspects of communities, but not species- the global ocean are unclear [13, 14]. In particular, we association patterns, which can also manifest the action do not know whether these crucial components of the of ecological processes. For example, selection exerted ocean microbiota are structured by the action of the by an environmental variable can drive species co- same or different ecological processes. Comprehending occurrences generating groups of highly associated spe- such processes is fundamental, as their differential action cies or modules in association networks that correspond can produce changes in the ocean microbiota compos- with specific environmental conditions [25]. Different ition that could impact global ecosystem function [15– members of these modules may be more abundant in 17]. A recent ecological synthesis explains the structure specific regions of the ocean, contributing to increase β- of communities and the emergence of biogeography as a diversity estimates between these regions when based on consequence of the action of four main processes: selec- standard compositional or phylogenetic β-diversity met- tion, dispersal, ecological drift and speciation [18]. Selec- rics. Yet, β-diversity estimates based on association- tion involves deterministic reproductive differences aware metrics may point to higher similarity between among individuals from different or the same species as these regions, as taxa belong to the same modules. Fur- a response to biotic or abiotic conditions. Selection can thermore, modules may display correlations with envir- act in two opposite directions; it can constrain (homoge- onmental heterogeneity. Thus, association aware metrics neous selection) or promote (heterogeneous selection) the of β-diversity may allow unveiling community patterns divergence of communities [19]. Dispersal is the move- and their relationships with environmental variables (i.e. ment of organisms across space, and rates can be high selection), which would be missed by standard ap- (homogenising dispersal), moderate, or low (dispersal proaches [26]. So far, most studies investigating the limitation)[19]. Dispersal limitation occurs when species structure of the ocean microbiota have not considered are absent from suitable habitats because potential species associations in their analyses of β-diversity. Logares et al. Microbiome (2020) 8:55 Page 3 of 17 The differential action of selection, dispersal and drift that appear to be driven by
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