Structural and functional characterization of Southern Ocean microbes

Abstract

Understanding the ecological patterns of microbiota in natural ecosystems is fundamental for predicting their responses to global change. As mediators of biogeochemical cycles, microbiota are essential for ecosystem functioning in the oceans. Estimates suggest that nearly half of the Earth’s net primary productivity occurs in the oceans. Yet surprisingly, the oceans are the least studied ecosystems. Physical oceanographic studies have shown that the Southern Ocean (SO) is a crucial marine carbon and heat storage. This research supports the solubility pump as the main driver of oceanographic processes in the SO. Recent studies on phytoplankton have shown the centrality of biological processes, but comparatively less is known regarding the role played by microorganisms. In this study, we performed a comprehensive analysis of the structure and function of SO microbial communities. We assessed microbiota from the epipelagic to the bathy- and abyssopelagic zones of the ocean, revealing remarkable insights regarding microbial community dynamics. The applications of several culture-independent techniques allowed us to substantially reduce the knowledge deficit regarding SO microbiomes and the effect of nutrient variables on their diversity and structure. The effect of an early spring phytoplankton bloom on the abundance, diversity, and structure of prokaryotes was assessed. Our results showed that an early spring bloom had limited effects on microbiota but increased total prokaryotic abundances in epipelagic waters. We also observed some compositional changes including an increase of Cyanobacteria. However, diversity and community structure remained consistent. Specific physicochemical parameters factors appear to drive microbial communities , including the availability of various nutrients and oceanographic variables determining SO water masses. Shotgun metagenomic sequencing allowed us to provide a compendium dataset of 628 metagenome-assembled genomes. Of these, 167 harboured chemolithoautotrophic potential. We show widespread distribution of chemolithoautotrophic bacteria and archaea along the aphotic water column, independent of the specific sampling depth, along all major SO fronts and zones. Inorganic carbon fixation coupled with the oxidation of reduced nutrients, such as thiosulfate and ammonia, were potentially key for biogeochemical cycling. Furthermore, a pangenome analysis suggest that genes for chemolithotrophy may be potentially exchanged between diverse bacteria and archaea through widespread horizontal gene transfer. These processes may be pivotal, especially in an ocean which absorbs 40% of anthropogenic derived CO2. Single cell-genomics was used to investigate chemolithoautotrophic SAR324. We show that SAR324, and associated phages, harbour genetic traits which are well-suited for nutrient sequestration in the abyssopelagic SO. SAR324 harbour a wide array of metabolic metabolisms. We provide the first report of putative SAR324 bacteriophages as well as CRISPR-Cas modules contained within SAR324 genomes. Auxiliary metabolic genes of large protein families were retrieved from SAR324 viral signatures, suggesting the role played by SAR324 phages towards biogeochemical cycling. The data from this study provides an enhanced understanding regarding microbial interactions along the water column in the SO. We show that these microbiota demonstrate depth-dependent resilient microbial structure. Further, the data highlight the importance of chemolithoautotrophic bacteria and archaea in the dark SO.