Abstract

The detailed lifestyle of microorganisms in deep-sea brine environments remains largely unexplored. Using a carefully calibrated genome binning approach, we reconstructed partial to nearly-complete genomes of 51 microorganisms in biofilms from the Thuwal cold seep brine pool of the Red Sea. The recovered metagenome-assembled genomes (MAGs) belong to six different phyla: Actinobacteria, Proteobacteria, Candidatus Cloacimonetes, Candidatus Marinimicrobia, Bathyarchaeota, and Thaumarchaeota. By comparison with close relatives of these microorganisms, we identified a number of unique genes associated with organic carbon metabolism and energy generation. These genes included various glycoside hydrolases, nitrate and sulfate reductases, putative bacterial microcompartment biosynthetic clusters (BMC), and F420H2 dehydrogenases. Phylogenetic analysis suggested that the acquisition of these genes probably occurred through horizontal gene transfer (HGT). Metatranscriptomics illustrated that glycoside hydrolases are among the most highly expressed genes. Our results suggest that the microbial inhabitants are well adapted to this brine environment, and anaerobic carbohydrate consumption mediated by glycoside hydrolases and electron transport systems (ETSs) is a dominant process performed by microorganisms from various phyla within this ecosystem.

Highlights

  • Microorganisms play important roles in the biogeochemical cycles of deep-sea environments, such as deep-sea hydrothermal vents and brine pools

  • Genome binning using two metagenomes, biofilm_Al and biofilm_PVC, generated 51 metagenome-assembled genomes (MAGs) of the biofilminhabited microorganisms (TCS1-51; “TCS” served as the abbreviation for “Thuwal cold seep”), including members of Actinobacteria, Gammaproteobacteria, Deltaproteobacteria, Epsilonprtoteobacteria, Candidatus Marinimicrobia, Candidatus Cloacimonetes, Bathyarchaeota and Thaumarchaeota (Table 1)

  • It is important to validate the results from genome binning, this approach has been repeatedly employed in various studies (Brown et al, 2015; Emerson et al, 2016)

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Summary

Introduction

Microorganisms play important roles in the biogeochemical cycles of deep-sea environments, such as deep-sea hydrothermal vents and brine pools. Studies of microbial lifestyles in brine pools are less common than those of hydrothermal vents. The brine pools studied so far include the Shaban Deep (Ferrer et al, 2012), Discovery Deep (Wang et al, 2013), Atlantis II Deep (Ngugi et al, 2015), and Kebrit Deep (Guan et al, 2015) of the Red Sea, which contains more than 25 deep hypersaline anoxic pools (Antunes et al, 2011). Brine pools probably share a common formation process of tectonically. Genomics of Deep-Sea Microorganisms induced brine formation, resulting in frequently observed high methane and sulfite fluxes (Faber et al, 1998). Despite the common origin and shared features of the investigated brine pools, regional variation may lead to distinct combinations of physicochemical parameters and sustains microorganisms with unique adaptive strategies

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