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

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,

Protistan plankton communities in the Galápagos Archipelago respond to changes in deep water masses resulting from the 2015/16 El Niño

“…Synechococcus flow cytometry cell counts were higher at western sites 3-7 in 2015 than 2016 (Supplementary Figure 3), similar to observations made at the same sites quantified using metagenomics (Gifford et al, 2020). Site four had the greatest difference between the years, having a concentration of 2.4×10 5 cells mL -1 in 2015 and 5.9 ×10 4 cells mL -1 in 2016.…”

“…El Niño conditions lead to reduced nitrate availability and decreases in Synechococcus, likely because of their high cellular nitrogen requirement (Moore et al, 2002), which allow small heterotrophic protists to dominate, altering marine food web dynamics in the EEP (Masotti et al, 2010). Contrary to community dynamics in the EEP, on the west side of the Galápagos Archipelago, Synechococcus and Prochlorococcus concentrations decreased during a neutral period of stronger upwelling following the 2015/16 El Niño (Gifford et al, 2020). Given that Prochlorococcus is speculated to prefer nitrogen sources other than nitrate, it may be more competitive under stratified El Niño conditions (Moore et al, 2002).…”

Synechococcusnitrogen gene loss in iron-limited ocean regions

“…Genome equivalents were enumerated by identifying single copy recombinase A (recA) genes in a metagenome sample, and then converted to volumetric abundances via recovery ratios derived from internal standards added prior to extraction (30)(31)(32)(33)(34)(35)(36)(37). A comparison between our quantitative metagenome-derived Synechococcus abundances and simultaneously collected flow cytometry Synechococcus cell concentrations show strong agreement (Fig.…”

Protistan plankton communities in the Galápagos Archipelago respond to changes in deep water masses resulting from the 2015/16 El Niño

“…Synechococcus flow cytometry cell counts were higher at western sites 3–7 in 2015 than in 2016 (Supporting Fig. 1), similar to observations made at the same sites quantified using metagenomics (Gifford et al ., 2020). Site 4 had the greatest difference between the years, having a concentration of 2.4 × 10 5 cells ml −1 in 2015 and 5.9 × 10 4 cells ml −1 in 2016.…”

“…El Niño conditions lead to reduced nitrate availability and decreases in Synechococcus , likely because of their high cellular nitrogen requirement (Moore et al ., 2002), which allow small heterotrophic protists to dominate, altering marine food web dynamics in the EEP (Masotti et al ., 2011). Contrary to community dynamics in the EEP, on the west side of the Galápagos Archipelago, Synechococcus and Prochlorococcus concentrations decreased during a neutral period of stronger upwelling following the 2015/16 El Niño (Gifford et al ., 2020). Given that Prochlorococcus is speculated to prefer nitrogen sources other than nitrate, it may be more competitive under stratified El Niño conditions (Moore et al ., 2002).…”