Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney

Magnetosome-producing microorganisms can sense and move toward the redox gradient and have been extensively studied in terrestrial and shallow marine sediment environments. However, given the difficulty of sampling, magnetotactic bacteria (MTB) are poorly explored in deep-sea hydrothermal fields. In...

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Main Authors: Shinsaku Nakano, Hitoshi Furutani, Shingo Kato, Mariko Kouduka, Toshitsugu Yamazaki, Yohey Suzuki
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1174899/full
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author Shinsaku Nakano
Hitoshi Furutani
Shingo Kato
Mariko Kouduka
Toshitsugu Yamazaki
Yohey Suzuki
author_facet Shinsaku Nakano
Hitoshi Furutani
Shingo Kato
Mariko Kouduka
Toshitsugu Yamazaki
Yohey Suzuki
author_sort Shinsaku Nakano
collection DOAJ
description Magnetosome-producing microorganisms can sense and move toward the redox gradient and have been extensively studied in terrestrial and shallow marine sediment environments. However, given the difficulty of sampling, magnetotactic bacteria (MTB) are poorly explored in deep-sea hydrothermal fields. In this study, a deep-sea hydrothermal vent chimney from the Southern Mariana Trough was collected using a remotely operated submersible. The mineralogical and geochemical characterization of the vent chimney sample showed an internal iron redox gradient. Additionally, the electron microscopy of particles collected by magnetic separation from the chimney sample revealed MTB cells with bullet-shaped magnetosomes, and there were minor occurrences of cuboctahedral and hexagonal prismatic magnetosomes. Genome-resolved metagenomic analysis was performed to identify microorganisms that formed magnetosomes. A metagenome-assembled genome (MAG) affiliated with Nitrospinae had magnetosome genes such as mamA, mamI, mamM, mamP, and mamQ. Furthermore, a diagnostic feature of MTB genomes, such as magnetosome gene clusters (MGCs), including mamA, mamP, and mamQ, was also confirmed in the Nitrospinae-affiliated MAG. Two lines of evidence support the occurrence of MTB in a deep-sea, inactive hydrothermal vent environment.
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spelling doaj.art-73d0a94862244abb86b5aede4f256fe12023-06-27T17:28:36ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-06-011410.3389/fmicb.2023.11748991174899Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimneyShinsaku Nakano0Hitoshi Furutani1Shingo Kato2Mariko Kouduka3Toshitsugu Yamazaki4Yohey Suzuki5Graduate School of Science, The University of Tokyo, Tokyo, JapanGraduate School of Science, The University of Tokyo, Tokyo, JapanJapan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Ibaraki, JapanGraduate School of Science, The University of Tokyo, Tokyo, JapanAtmosphere and Ocean Research Institute, The University of Tokyo, Chiba, JapanGraduate School of Science, The University of Tokyo, Tokyo, JapanMagnetosome-producing microorganisms can sense and move toward the redox gradient and have been extensively studied in terrestrial and shallow marine sediment environments. However, given the difficulty of sampling, magnetotactic bacteria (MTB) are poorly explored in deep-sea hydrothermal fields. In this study, a deep-sea hydrothermal vent chimney from the Southern Mariana Trough was collected using a remotely operated submersible. The mineralogical and geochemical characterization of the vent chimney sample showed an internal iron redox gradient. Additionally, the electron microscopy of particles collected by magnetic separation from the chimney sample revealed MTB cells with bullet-shaped magnetosomes, and there were minor occurrences of cuboctahedral and hexagonal prismatic magnetosomes. Genome-resolved metagenomic analysis was performed to identify microorganisms that formed magnetosomes. A metagenome-assembled genome (MAG) affiliated with Nitrospinae had magnetosome genes such as mamA, mamI, mamM, mamP, and mamQ. Furthermore, a diagnostic feature of MTB genomes, such as magnetosome gene clusters (MGCs), including mamA, mamP, and mamQ, was also confirmed in the Nitrospinae-affiliated MAG. Two lines of evidence support the occurrence of MTB in a deep-sea, inactive hydrothermal vent environment.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1174899/fullmagnetotactic bacteriaNitrospinae-related sequencesmagnetosome gene clusterredox gradientelectron microscopy
spellingShingle Shinsaku Nakano
Hitoshi Furutani
Shingo Kato
Mariko Kouduka
Toshitsugu Yamazaki
Yohey Suzuki
Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney
Frontiers in Microbiology
magnetotactic bacteria
Nitrospinae-related sequences
magnetosome gene cluster
redox gradient
electron microscopy
title Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney
title_full Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney
title_fullStr Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney
title_full_unstemmed Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney
title_short Bullet-shaped magnetosomes and metagenomic-based magnetosome gene profiles in a deep-sea hydrothermal vent chimney
title_sort bullet shaped magnetosomes and metagenomic based magnetosome gene profiles in a deep sea hydrothermal vent chimney
topic magnetotactic bacteria
Nitrospinae-related sequences
magnetosome gene cluster
redox gradient
electron microscopy
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1174899/full
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