Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes

Electrochemically active biofilms are capable of exchanging electrons with solid electron acceptors and have many energy and environmental applications such as bioelectricity generation and environmental remediation. The performance of electrochemically active biofilms is usually dependent on c-type...

Full description

Saved in:
Bibliographic Details
Main Authors: Ng, Chun Kiat, Xu, Jiabao, Cai, Zhao, Yang, Liang, Thompson, Ian P., Huang, Wei E., Cao, Bin
Other Authors: School of Civil and Environmental Engineering
Format: Article
Language:English
Published: 2021
Subjects:
Online Access:https://hdl.handle.net/10356/148783
Tags: Add Tag
No Tags, Be the first to tag this record!
Institution: Nanyang Technological University
Language: English
id sg-ntu-dr.10356-148783
record_format dspace
spelling sg-ntu-dr.10356-1487832021-05-15T20:11:24Z Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes Ng, Chun Kiat Xu, Jiabao Cai, Zhao Yang, Liang Thompson, Ian P. Huang, Wei E. Cao, Bin School of Civil and Environmental Engineering Singapore Centre for Environmental Life Sciences and Engineering Engineering::Bioengineering Cytochrome Cyclic Electrochemically active biofilms are capable of exchanging electrons with solid electron acceptors and have many energy and environmental applications such as bioelectricity generation and environmental remediation. The performance of electrochemically active biofilms is usually dependent on c-type cytochromes, while biofilm development is controlled by a signal cascade mediated by the intracellular secondary messenger bis-(3'-5') cyclic dimeric guanosine monophosphate (c-di-GMP). However, it is unclear whether there are any links between the c-di-GMP regulatory system and the expression of c-type cytochromes. In this study, we constructed a S. oneidensis MR-1 strain with a higher cytoplasmic c-di-GMP level by constitutively expressing a c-di-GMP synthase and it exhibited expected c-di-GMP-influenced traits, such as lowered motility and increased biofilm formation. Compared to MR-1 wild-type strain, the high c-di-GMP strain had a higher Fe(III) reduction rate (21.58 vs 11.88 pM of Fe(III)/h cell) and greater expression of genes that code for the proteins involved in the Mtr pathway, including CymA, MtrA, MtrB, MtrC and OmcA. Furthermore, single-cell Raman microspectroscopy (SCRM) revealed a great increase of c-type cytochromes in the high c-di-GMP strain as compared to MR-1 wild-type strain. Our results reveal for the first time that the c-di-GMP regulation system indirectly or directly positively regulates the expression of cytochromes involved in the extracellular electron transport (EET) in S. oneidensis, which would help to understand the regulatory mechanism of c-di-GMP on electricity production in bacteria. Ministry of Education (MOE) Nanyang Technological University National Research Foundation (NRF) Published version B. Cao acknowledges financial support from the Ministry of Education (MOE) Academic Research Fund (AcRF) Tier 2 Grant (MOE2017‐T2‐2‐042) and the National Research Foundation and MOE Singapore under its Research Centre of Excellence Programme, Singapore Centre for Environmental Life Sciences Engineering (SCELSE) (M4330005.C70), Nanyang Technological University, Singapore. W. E. Huang acknowledges financial and instrumentational support from EPSRC (Grants EP/M002403/1 and EP/M02833X/1) and NERC (Grant NE/M002934/1). 2021-05-12T07:59:53Z 2021-05-12T07:59:53Z 2020 Journal Article Ng, C. K., Xu, J., Cai, Z., Yang, L., Thompson, I. P., Huang, W. E. & Cao, B. (2020). Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes. Microbial Biotechnology, 13(6), 1904-1916. https://dx.doi.org/10.1111/1751-7915.13636 1751-7915 0000-0002-1723-9988 0000-0002-1285-9408 0000-0002-2362-0128 0000-0003-1302-6528 0000-0002-9462-496X https://hdl.handle.net/10356/148783 10.1111/1751-7915.13636 32729223 2-s2.0-85088788170 6 13 1904 1916 en MOE2017-T2-2-042 M4330005.C70 EP/M002403/1 EP/M02833X/1 NE/M002934/1 Microbial Biotechnology © 2020 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Engineering::Bioengineering
Cytochrome
Cyclic
spellingShingle Engineering::Bioengineering
Cytochrome
Cyclic
Ng, Chun Kiat
Xu, Jiabao
Cai, Zhao
Yang, Liang
Thompson, Ian P.
Huang, Wei E.
Cao, Bin
Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes
description Electrochemically active biofilms are capable of exchanging electrons with solid electron acceptors and have many energy and environmental applications such as bioelectricity generation and environmental remediation. The performance of electrochemically active biofilms is usually dependent on c-type cytochromes, while biofilm development is controlled by a signal cascade mediated by the intracellular secondary messenger bis-(3'-5') cyclic dimeric guanosine monophosphate (c-di-GMP). However, it is unclear whether there are any links between the c-di-GMP regulatory system and the expression of c-type cytochromes. In this study, we constructed a S. oneidensis MR-1 strain with a higher cytoplasmic c-di-GMP level by constitutively expressing a c-di-GMP synthase and it exhibited expected c-di-GMP-influenced traits, such as lowered motility and increased biofilm formation. Compared to MR-1 wild-type strain, the high c-di-GMP strain had a higher Fe(III) reduction rate (21.58 vs 11.88 pM of Fe(III)/h cell) and greater expression of genes that code for the proteins involved in the Mtr pathway, including CymA, MtrA, MtrB, MtrC and OmcA. Furthermore, single-cell Raman microspectroscopy (SCRM) revealed a great increase of c-type cytochromes in the high c-di-GMP strain as compared to MR-1 wild-type strain. Our results reveal for the first time that the c-di-GMP regulation system indirectly or directly positively regulates the expression of cytochromes involved in the extracellular electron transport (EET) in S. oneidensis, which would help to understand the regulatory mechanism of c-di-GMP on electricity production in bacteria.
author2 School of Civil and Environmental Engineering
author_facet School of Civil and Environmental Engineering
Ng, Chun Kiat
Xu, Jiabao
Cai, Zhao
Yang, Liang
Thompson, Ian P.
Huang, Wei E.
Cao, Bin
format Article
author Ng, Chun Kiat
Xu, Jiabao
Cai, Zhao
Yang, Liang
Thompson, Ian P.
Huang, Wei E.
Cao, Bin
author_sort Ng, Chun Kiat
title Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes
title_short Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes
title_full Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes
title_fullStr Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes
title_full_unstemmed Elevated intracellular cyclic-di-GMP level in Shewanella oneidensis increases expression of c-type cytochromes
title_sort elevated intracellular cyclic-di-gmp level in shewanella oneidensis increases expression of c-type cytochromes
publishDate 2021
url https://hdl.handle.net/10356/148783
_version_ 1701270544607870976