Abstract
The “Latescibacteria” (formerly WS3), member of the Fibrobacteres–Chlorobi–Bacteroidetes (FCB) superphylum, represents a ubiquitous candidate phylum found in terrestrial, aquatic, and marine ecosystems. Recently, single-cell amplified genomes (SAGs) representing the “Latescibacteria” were obtained from the anoxic monimolimnion layers of Sakinaw Lake (British Columbia, Canada), and anoxic sediments of a coastal lagoon (Etoliko lagoon, Western Greece). Here, we present a detailed in-silico analysis of the four SAGs to gain some insights on their metabolic potential and apparent ecological roles. Metabolic reconstruction suggests an anaerobic fermentative mode of metabolism, as well as the capability to degrade multiple polysaccharides and glycoproteins that represent integral components of green (Charophyta and Chlorophyta) and brown (Phaeophycaea) algae cell walls (pectin, alginate, ulvan, fucan, hydroxyproline-rich glycoproteins), storage molecules (starch and trehalose), and extracellular polymeric substances (EPSs). The analyzed SAGs also encode dedicated transporters for the uptake of produced sugars and amino acids/oligopeptides, as well as an extensive machinery for the catabolism of all transported sugars, including the production of a bacterial microcompartment (BMC) to sequester propionaldehyde, a toxic intermediate produced during fucose and rhamnose metabolism. Finally, genes for the formation of gas vesicles, flagella, type IV pili, and oxidative stress response were found, features that could aid in cellular association with algal detritus. Collectively, these results indicate that the analyzed “Latescibacteria” mediate the turnover of multiple complex organic polymers of algal origin that reach deeper anoxic/microoxic habitats in lakes and lagoons. The implications of such process on our understanding of niche specialization in microbial communities mediating organic carbon turnover in stratified water bodies are discussed.
Highlights
Over the past few decades, small subunit ribosomal RNA (SSU or 16S rRNA) gene-based surveys have prompted a drastic reevaluation of the scope of phylum level diversity within the domain Bacteria
Our analysis suggests that the “Latescibacteria” recovered from Sakinaw Lake and Etoliko lagoon transform algal detritus sinking from sunlit surface waters into fermentation products with the potential to contribute to microbial food webs in anaerobic waters below
Our analysis of four “Latescibacteria” single-cell amplified genomes (SAGs) obtained from the anaerobic monimolimnion water column of Sakinaw Lake, and the anaerobic sediments of Etoliko lagoon revealed extensive saccharolytic and proteolytic capabilities, with preference for specific polysaccharides and glycoproteins such as pectins, alginates, fucans, ulvans, xyloglucans, starch, extensins, and arabinogalactan protein originating from algal cell walls and extracellular polymeric substances (EPSs)
Summary
Over the past few decades, small subunit ribosomal RNA (SSU or 16S rRNA) gene-based surveys have prompted a drastic reevaluation of the scope of phylum level diversity within the domain Bacteria. Recent advances in cell sorting and whole genome amplification and assembly have facilitated the acquisition of single-cell amplified genomes (SAGs) derived from numerous candidate phyla [8,9,10,11,12,13,14,15,16] Metabolic reconstruction with these SAGs provides a unique opportunity to uncover the ecological and biogeochemical roles played by these enigmatic microbial groups. One such candidate phylum is WS3 (Wurtsmith aquifer Sequences-3), whose members were first identified in a 16S rRNA gene-based survey of anoxic sediments obtained from a hydrocarbon- and chlorinated-solvents-contaminated aquifer in northern Michigan, USA in 1998 [17]. The name “Latescibacteria” (hiding small rods) was suggested for the candidate phylum
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