Global Distribution Patterns and Pangenomic Diversity of the Candidate Phylum “Latescibacteria” (WS3)

We investigated the global distribution patterns and pangenomic diversity of the candidate phylum “Latescibacteria ” (WS3) in 16S rRNA gene as well as metagenomic data sets. We document distinct distribution patterns for various “Latescibacteria ” orders in 16S rRNA gene data sets, with prevalence of orders sediment_1 in terrestrial, PBSIII_9 in groundwater and temperate freshwater, and GN03 in pelagic marine, saline-hypersaline, and wastewater habitats. Using a fragment recruitment approach, we identified 68.9 Mb of “Latescibacteria ”-affiliated contigs in publicly available metagenomic data sets comprising 73,079 proteins. Metabolic reconstruction suggests a prevalent saprophytic lifestyle in all “Latescibacteria ” orders, with marked capacities for the degradation of proteins, lipids, and polysaccharides predominant in plant, bacterial, fungal/crustacean, and eukaryotic algal cell walls. As well, extensive transport and central metabolic pathways for the metabolism of imported monomers were identified. Interestingly, genes and domains suggestive of the production of a cellulosome—e.g., protein-coding genes harboring dockerin I domains attached to a glycosyl hydrolase and scaffoldin-encoding genes harboring cohesin I and CBM37 domains—were identified in order PBSIII_9, GN03, and MSB-4E2 fragments recovered from four anoxic aquatic habitats; hence extending the cellulosomal production capabilities inBacteria beyond the Gram-positiveFirmicutes . In addition to fermentative pathways, a complete electron transport chain with terminal cytochromec oxidases Caa3 (for operation under high oxygen tension) and Cbb3 (for operation under low oxygen tension) were identified in PBSIII_9 and GN03 fragments recovered from oxygenated and partially/seasonally oxygenated aquatic habitats. Our metagenomic recruitment effort hence represents a comprehensive pangenomic view of this yet-uncultured phylum and provides insights broader than and complementary to those gained from genome recovery initiatives focusing on a single or few sampled environments.IMPORTANCE Our understanding of the phylogenetic diversity, metabolic capabilities, and ecological roles of yet-uncultured microorganisms is rapidly expanding. However, recent efforts mainly have been focused on recovering genomes of novel microbial lineages from a specific sampling site, rather than from a wide range of environmental habitats. To comprehensively evaluate the genomic landscape, putative metabolic capabilities, and ecological roles of yet-uncultured candidate phyla, efforts that focus on the recovery of genomic fragments from a wide range of habitats and that adequately sample the intraphylum diversity within a specific target lineage are needed. Here, we investigated the global distribution patterns and pangenomic diversity of the candidate phylum “Latescibacteria .” Our results document the preference of specific “Latescibacteria ” orders to specific habitats, the prevalence of plant polysaccharide degradation abilities within all “Latescibacteria ” orders, the occurrence of all genes/domains necessary for the production of cellulosomes within three “Latescibacteria ” orders (GN03, PBSIII_9, and MSB-4E2) in data sets recovered from anaerobic locations, and the identification of the components of an aerobic respiratory chain, as well as occurrence of multiple O2 -dependent metabolic reactions in “Latescibacteria ” orders GN03 and PBSIII_9 recovered from oxygenated habitats. The results demonstrate the value of phylocentric pangenomic surveys for understanding the global ecological distribution and panmetabolic abilities of yet-uncultured microbial lineages since they provide broader and more complementary insights than those gained from single-cell genomic and/or metagenomic-enabled genome recovery efforts focusing on a single sampling site.