Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical ‘copper switch’
Abstract
Copper is an important component of methanotrophic physiology as it controls the expression and activity of alternative forms of methane monooxygenase (MMO). To collect copper, some methanotrophs secrete a chalkophore or copper-binding compound called methanobactin (MB). MB is a ribosomally synthesized post-translationally modified polypeptide (RiPP) that, after binding copper, is collected by MbnT, a TonB-dependent transporter (TBDT). Structurally different forms of MB have been characterized, and here we show that different forms of MB are collected by specific TBDTs. Further, we report that in the model methanotroph, Methylosinus trichosporium OB3b, expression of the TBDT required for uptake of a different MB made by Methylocystis sp. strain SB2 (MB-SB2), is induced in the presence of MB-SB2, suggesting that methanotrophs have developed specific machinery and regulatory systems to actively take up MB from other methanotrophs for copper collection. Moreover, the canonical “copper-switch” in Ms. trichosporium OB3b that controls expression of alternative MMOs is apparent if one of the two TBDTs required for MB-OB3b and MB-SB2 uptake is knocked out, but is disrupted if both TBDTs are knocked out. Furthermore, these data indicate that MB uptake, including the uptake of exogenous MB, plays an important role in the copper switch in M. trichosporiummore »
- Authors:
-
- Univ. of Michigan, Ann Arbor, MI (United States)
- Iowa State Univ., Ames, IA (United States)
- Publication Date:
- Research Org.:
- Univ. of Michigan, Ann Arbor, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1838664
- Grant/Contract Number:
- SC0020174; AC52-07NA27344
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 88; Journal Issue: 1; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; copper; methanobactin; TonB-dependent transporters; methane; methanotrophs; methanotrophy; microbial interactions; chalkophore
Citation Formats
Peng, Peng, Kang-Yun, Christina S., Chang, Jin, Gu, Wenyu, DiSpirito, Alan A., and Semrau, Jeremy D. Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical ‘copper switch’. United States: N. p., 2021.
Web. doi:10.1128/aem.01793-21.
Peng, Peng, Kang-Yun, Christina S., Chang, Jin, Gu, Wenyu, DiSpirito, Alan A., & Semrau, Jeremy D. Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical ‘copper switch’. United States. https://doi.org/10.1128/aem.01793-21
Peng, Peng, Kang-Yun, Christina S., Chang, Jin, Gu, Wenyu, DiSpirito, Alan A., and Semrau, Jeremy D. Wed .
"Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical ‘copper switch’". United States. https://doi.org/10.1128/aem.01793-21. https://www.osti.gov/servlets/purl/1838664.
@article{osti_1838664,
title = {Two TonB-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical ‘copper switch’},
author = {Peng, Peng and Kang-Yun, Christina S. and Chang, Jin and Gu, Wenyu and DiSpirito, Alan A. and Semrau, Jeremy D.},
abstractNote = {Copper is an important component of methanotrophic physiology as it controls the expression and activity of alternative forms of methane monooxygenase (MMO). To collect copper, some methanotrophs secrete a chalkophore or copper-binding compound called methanobactin (MB). MB is a ribosomally synthesized post-translationally modified polypeptide (RiPP) that, after binding copper, is collected by MbnT, a TonB-dependent transporter (TBDT). Structurally different forms of MB have been characterized, and here we show that different forms of MB are collected by specific TBDTs. Further, we report that in the model methanotroph, Methylosinus trichosporium OB3b, expression of the TBDT required for uptake of a different MB made by Methylocystis sp. strain SB2 (MB-SB2), is induced in the presence of MB-SB2, suggesting that methanotrophs have developed specific machinery and regulatory systems to actively take up MB from other methanotrophs for copper collection. Moreover, the canonical “copper-switch” in Ms. trichosporium OB3b that controls expression of alternative MMOs is apparent if one of the two TBDTs required for MB-OB3b and MB-SB2 uptake is knocked out, but is disrupted if both TBDTs are knocked out. Furthermore, these data indicate that MB uptake, including the uptake of exogenous MB, plays an important role in the copper switch in M. trichosporium OB3b and thus overall activity. Based on these data, we propose a revised model for the “copper-switch” in this methanotroph that involves MB uptake.},
doi = {10.1128/aem.01793-21},
journal = {Applied and Environmental Microbiology},
number = 1,
volume = 88,
place = {United States},
year = {Wed Oct 20 00:00:00 EDT 2021},
month = {Wed Oct 20 00:00:00 EDT 2021}
}
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