Cargando…
Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field
The Methyloprofundus 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 Methyloprofundus variants in the Iheya North deep-sea...
Autores principales: | , , , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8788690/ https://www.ncbi.nlm.nih.gov/pubmed/34788070 http://dx.doi.org/10.1128/AEM.00758-21 |
_version_ | 1784639614628134912 |
---|---|
author | 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 |
author_facet | 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 |
author_sort | Hirayama, Hisako |
collection | PubMed |
description | The Methyloprofundus 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 Methyloprofundus 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 (pmoA) detected 647 amplicon sequence variants (ASVs) of the Methyloprofundus clade in microbial communities newly formed in in situ 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 Methyloprofundus 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 Methyloprofundus 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. IMPORTANCE 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 “Bathymodiolus” platifrons 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 Methyloprofundus 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 indicated that it corresponds to a new species in the genus Methyloprofundus. This species might be a dominant member of the indigenous Methyloprofundus population. New information on free-living Methyloprofundus populations suggests that the hydrothermal field is a promising locale at which to investigate the adaptive capacity and associated genetic diversity of Methyloprofundus spp. |
format | Online Article Text |
id | pubmed-8788690 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-87886902022-07-25 Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field 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 Appl Environ Microbiol Environmental Microbiology The Methyloprofundus 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 Methyloprofundus 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 (pmoA) detected 647 amplicon sequence variants (ASVs) of the Methyloprofundus clade in microbial communities newly formed in in situ 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 Methyloprofundus 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 Methyloprofundus 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. IMPORTANCE 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 “Bathymodiolus” platifrons 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 Methyloprofundus 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 indicated that it corresponds to a new species in the genus Methyloprofundus. This species might be a dominant member of the indigenous Methyloprofundus population. New information on free-living Methyloprofundus populations suggests that the hydrothermal field is a promising locale at which to investigate the adaptive capacity and associated genetic diversity of Methyloprofundus spp. American Society for Microbiology 2022-01-25 /pmc/articles/PMC8788690/ /pubmed/34788070 http://dx.doi.org/10.1128/AEM.00758-21 Text en Copyright © 2022 Hirayama et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Environmental Microbiology 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 Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field |
title | Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field |
title_full | Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field |
title_fullStr | Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field |
title_full_unstemmed | Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field |
title_short | Multispecies Populations of Methanotrophic Methyloprofundus and Cultivation of a Likely Dominant Species from the Iheya North Deep-Sea Hydrothermal Field |
title_sort | multispecies populations of methanotrophic methyloprofundus and cultivation of a likely dominant species from the iheya north deep-sea hydrothermal field |
topic | Environmental Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8788690/ https://www.ncbi.nlm.nih.gov/pubmed/34788070 http://dx.doi.org/10.1128/AEM.00758-21 |
work_keys_str_mv | AT hirayamahisako multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT takakiyoshihiro multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT abemariko multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT imachihiroyuki multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT ikutatetsuro multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT miyazakijunichi multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT tasumieiji multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT uematsukatsuyuki multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT tameakihiro multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT tsudamiwako multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT tanakakeiko multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT matsuiyohei multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT watanabehiromikayama multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT yamamotohiroyuki multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield AT takaiken multispeciespopulationsofmethanotrophicmethyloprofundusandcultivationofalikelydominantspeciesfromtheiheyanorthdeepseahydrothermalfield |