Dominance of Sulfurospirillum in Metagenomes Associated with the Methane Ice Worm (Sirsoe methanicola)

• Published in: Applied and environmental microbiology Vol. 88; no. 15; p. e0029022
• Main Authors: Lim, Shen Jean, Thompson, Luke R, Young, Craig M, Gaasterland, Terry, Goodwin, Kelly D
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 09.08.2022
• Subjects: Amino acids; Animals; Bacteria; Biosynthesis; Carbon; Carbon - metabolism; Carbon compounds; Disproportionation; Energy reserves; Genomes; Host-Microbial Interactions; Humans; Hydrates; Ice worms; Invertebrate Microbiology; Metagenome; Metagenomics; Methane; Methane - metabolism; Methane hydrates; Microorganisms; Nutritive value; Organic carbon; Phylogeny; Polychaeta - metabolism; RNA, Ribosomal, 16S - genetics; RNA, Ribosomal, 16S - metabolism; rRNA 16S; Spotlight Selection; Sulfides - metabolism; Sulfur; Sulfurospirillum; Taxa; Tetrathionate; Vitamin B12; invertebrate microbiology; polychaete; methane hydrate; worm; metagenomics; Gulf of Mexico; deep-sea; host-microbial interactions; microbiome; Sulfurospirillum
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/aem.00290-22

Sirsoe methanicola, commonly known as the methane ice worm, is the only macrofaunal species known to inhabit the Gulf of Mexico methane hydrates. Little is known about this elusive marine polychaete that can colonize rich carbon and energy reserves. Metagenomic analysis of gut contents and worm fragments predicted diverse metabolic capabilities with the ability to utilize a range of nitrogen, sulfur, and organic carbon compounds through microbial taxa affiliated with , , , , , and . and were additionally identified from extracted full-length 16S rRNA sequences, and read analysis identified 196 bacterial families. Overall, the microbial community appeared dominated by uncultured , a taxon previously considered free-living rather than host-associated. Metagenome-assembled genomes (MAGs) classified as uncultured predicted thiosulfate disproportionation and the reduction of tetrathionate, sulfate, sulfide/polysulfide, and nitrate. Microbial amino acid and vitamin B12 biosynthesis genes were identified in multiple MAGs, suggesting nutritional value to the host. Reads assigned to aerobic or anaerobic methanotrophic taxa were rare. Methane hydrates represent vast reserves of natural gas with roles in global carbon cycling and climate change. This study provided the first analysis of metagenomes associated with Sirsoe methanicola, the only polychaete species known to colonize methane hydrates. Previously unrecognized participation of in a gut microbiome is provided, and the role of sulfur compound redox reactions within this community is highlighted. The comparative biology of S. methanicola is of general interest given research into the adverse effects of sulfide production in human gut microbiomes. In addition, taxonomic assignments are provided for nearly 200 bacterial families, expanding our knowledge of microbiomes in the deep sea.