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

• Published in: Applied and environmental microbiology Vol. 83; no. 10; p. E00521
• Main Authors: Farag, Ibrahim F, Youssef, Noha H, Elshahed, Mostafa S
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 01.05.2017
• Subjects: Algae; Aquatic habitats; Bacteria; Bacteria - classification; Bacteria - genetics; Bacteria - isolation & purification; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Biodegradation; Cell walls; Cellulosomes - genetics; Cellulosomes - metabolism; Coding; Cohesin; Cohesion; Cytochrome; Cytochrome c; Datasets; Degradation; DNA, Bacterial - genetics; Ecosystem; Electron transport; Electron transport chain; Evolutionary and Genomic Microbiology; Firmicutes; Fragmentation; Fragments; Fresh Water - microbiology; Fungi; Genes; Genetic Variation; Genomes; Genomics; Glycosyl hydrolase; Groundwater; Groundwater - microbiology; Habitats; Hydrolase; Lipids; Metabolic pathways; Metabolism; Monomers; Oxygen; Oxygen tension; Phylogeny; Polysaccharides; Proteins; Reconstruction; Recovery; Ribonucleic acid; RNA; RNA, Ribosomal, 16S - genetics; rRNA 16S; Saccharides; Shellfish; Spotlight; Tension; Terrestrial environments; Transcription; Walls; Wastewater; Latescibacteria; cellulosome; metagenomics
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/AEM.00521-17

We investigated the global distribution patterns and pangenomic diversity of the candidate phylum " " (WS3) in 16S rRNA gene as well as metagenomic data sets. We document distinct distribution patterns for various " " 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 " "-affiliated contigs in publicly available metagenomic data sets comprising 73,079 proteins. Metabolic reconstruction suggests a prevalent saprophytic lifestyle in all " " 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 in beyond the Gram-positive In addition to fermentative pathways, a complete electron transport chain with terminal cytochrome 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. 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 " " Our results document the preference of specific " " orders to specific habitats, the prevalence of plant polysaccharide degradation abilities within all " " orders, the occurrence of all genes/domains necessary for the production of cellulosomes within three " " 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 O -dependent metabolic reactions in " " 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.