Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field

The clade is represented by uncultivated methanotrophic bacterial endosymbionts of deep-sea bathymodiolin mussels, but only a single free-living species has been cultivated to date. This study reveals the existence of free-living variants in the Iheya North deep-sea hydrothermal field in the mid-Oki...

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Published in:Applied and environmental microbiology 2022-01, Vol.88 (2), p.e0075821-e0075821
Main Authors: Hirayama, Hisako, Takaki, Yoshihiro, Abe, Mariko, Imachi, Hiroyuki, Ikuta, Tetsuro, Miyazaki, Junichi, Tasumi, Eiji, Uematsu, Katsuyuki, Tame, Akihiro, Tsuda, Miwako, Tanaka, Keiko, Matsui, Yohei, Watanabe, Hiromi Kayama, Yamamoto, Hiroyuki, Takai, Ken
Format: Article
Language:English
Subjects:
Aldolase
Animals
Biofilms
Chemotaxis
Colonization
Cultivation
Deep sea
Deep sea environments
Denitrification
Dominant species
Endosymbionts
Environmental Microbiology
Fructose
Fructose-1,6-diphosphate
Fructose-6-phosphate
Fructose-6-phosphate aldolase
Glycolysis
Hypoxia
Methane
Methane - metabolism
Methane monooxygenase
Methanol dehydrogenase
Methylococcaceae - genetics
Methylococcaceae - metabolism
Microbial activity
Microbiota
Microorganisms
Mollusks
Mussels
Mytilidae - microbiology
Phylogeny
RNA, Ribosomal, 16S - genetics
Shellfish
Species classification
Symbiosis
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Summary:The clade is represented by uncultivated methanotrophic bacterial endosymbionts of deep-sea bathymodiolin mussels, but only a single free-living species has been cultivated to date. This study reveals the existence of free-living variants in the Iheya North deep-sea hydrothermal field in the mid-Okinawa Trough. A clade-targeted amplicon analysis of the particulate methane monooxygenase gene ( ) detected 647 amplicon sequence variants (ASVs) of the clade in microbial communities newly formed in colonization systems. Such systems were deployed at colonies of bathymodiolin mussels and a galatheoid crab in diffuse-flow areas. These ASVs were classified into 161 species-like groups. The proportion of the species-like groups representing endosymbionts of mussels was unexpectedly low. A methanotrophic bacterium designated INp10, a likely dominant species in the population in this field, was enriched in a biofilm formed in a methane-fed cultivation system operated at 10°C. Genomic characterization with the gene transcription data set of INp10 from the biofilm suggested traits advantageous to niche competition in environments, such as mobility, chemotaxis, biofilm formation, offensive and defensive systems, and hypoxia tolerance. The notable metabolic traits that INp10 shares with some members are the use of lanthanide-dependent XoxF as the sole methanol dehydrogenase due to the absence of the canonical MxaFI, the glycolytic pathway using fructose-6-phosphate aldolase instead of fructose-1,6-bisphosphate aldolase, and the potential to perform partial denitrification from nitrate under oxygen-limited conditions. These findings help us better understand the ecological strategies of this possibly widespread marine-specific methanotrophic clade. The Iheya North deep-sea hydrothermal field in the mid-Okinawa Trough is characterized by abundant methane derived from organic-rich sediments and diverse chemosynthetic animal species, including those harboring methanotrophic bacterial symbionts, such as bathymodiolin mussels Bathymodiolus japonicus and " " and a galatheoid crab, Shinkaia crosnieri. Symbiotic methanotrophs have attracted significant attention, and yet free-living methanotrophs in this environment have not been studied in detail. We focused on the free-living spp. that thrive in this hydrothermal field and identified an unexpectedly large number of species-like groups in this clade. Moreover, we enriched and characterized a methanotroph whose genome sequence in
ISSN:0099-2240
1098-5336
DOI:10.1128/AEM.00758-21