Microbial Niche Diversification in the Galápagos Archipelago and Its Response to El Niño.

Scott M Gifford,Adrian Marchetti,Patricia M Medeiros,Liang Zhao,Harvey Seim,Kimberly Delong,Brooke Stemple

doi:10.3389/fmicb.2020.575194

Abstract

The Galápagos Archipelago is located at the intersection of several major oceanographic features that produce diverse environmental conditions around the islands, and thus has the potential to serve as a natural laboratory for discerning the underlying environmental factors that structure marine microbial communities. Here we used quantitative metagenomics to characterize microbial communities in relation to archipelago marine habitats, and how those populations shift due to substantial environmental changes brought on by El Niño. Environmental conditions such as temperature, salinity, inorganic dissolved nutrients, and dissolved organic carbon (DOC) concentrations varied throughout the archipelago, revealing a diversity of potential microbial niches arising from upwelling, oligotrophic to eutrophic gradients, physical isolation, and potential island mass effects. The volumetric abundances of microbial community members shifted with these environmental changes and revealed several taxonomic indicators of different water masses. This included a transition from a Synechococcus dominated system in the west to an even mix of Synechococcus and Prochlorococcus in the east, mirroring the archipelago’s mesotrophic to oligotrophic and productivity gradients. Several flavobacteria groups displayed characteristic habitat distributions, including enrichment of Polaribacter and Tenacibaculum clades in the relatively nutrient rich western waters, Leeuwenhoekiella spp. that were enriched in the more nutrient-deplete central and eastern sites, and the streamlined MS024-2A group found to be abundant across all sites. During the 2015/16 El Niño event, both environmental conditions and microbial community composition were substantially altered, primarily on the western side of the archipelago due to the reduction of upwelling from the Equatorial Undercurrent. When the upwelling resumed, concentrations of inorganic nutrients and DOC at the western surface sites were more typical of mesopelagic depths. Correspondingly, Synechococcus abundances decreased by an order of magnitude, while groups associated with deeper water masses were enriched, including streamlined roseobacters HTCC2255 and HIMB11, Thioglobacaceae, methylotrophs (Methylophilaceae), archaea (Nitrosopumilaceae), and distinct subpopulations of Pelagibaceriales (SAR11 clade). These results provide a quantitative framework to connect community-wide microbial volumetric abundances to their environmental drivers, and thus incorporation into biogeochemical and ecological models.

Highlights

Microbes mediate the flux of energy and materials through the ocean (Moran, 2015), yet how environmental conditions structure marine microbial communities, and the suite of biogeochemical and ecological activities they carry out, is only partially understood (Fuhrman et al, 2015; Mende et al, 2017)
Surface waters (5–10 m) spanning the Galápagos Archipelago were sampled in October 2015 and 2016 (Figure 1A), encompassing a range of environmental conditions (Figure 1E)
Western stations had the coldest and most nutrient rich surface waters, owing to the upwelling of the Equatorial Undercurrent (EUC) as it collides with the archipelago platform (Liu et al, 2014)

Summary

Introduction

Microbes mediate the flux of energy and materials through the ocean (Moran, 2015), yet how environmental conditions structure marine microbial communities, and the suite of biogeochemical and ecological activities they carry out, is only partially understood (Fuhrman et al, 2015; Mende et al, 2017). Darwin’s observations of differences in the Galápagos terrestrial habitats and their associated fauna were critical to development of the theory of speciation through natural selection. In contrast to these terrestrial ecosystems, identifying the factors structuring marine microbial communities is less obvious given marine environments are well mixed with low barriers to nutrient and organism exchange. The Galápagos Archipelago is located in a unique oceanographic setting in which several major oceanographic features intersect to create diverse marine habitats with gradients in temperature, inorganic dissolved nutrients, primary production, organic matter composition and concentration, and plankton groups in a relatively close proximity (Jimenez, 1981; Liu et al, 2014; Campoverde et al, 2018) that might make it well suited for identifying marine microbial niche diversification. The archipelago has substantially higher rates of primary production than the surrounding oligotrophic waters of the East Equatorial Pacific (Figure 1C)

Methods

Results

Conclusion