Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>

ABSTRACT The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing...

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Autores principales:	Haijian Du, Wenyan Zhang, Wensi Zhang, Weijia Zhang, Hongmiao Pan, Yongxin Pan, Dennis A. Bazylinski, Long-Fei Wu, Tian Xiao, Wei Lin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Terasakiella evolution gene duplication genomes magnetosome gene cluster magnetotactic bacteria Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bb5ed295422744fa891fbf8ca6499cb9
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spelling	oai:doaj.org-article:bb5ed295422744fa891fbf8ca6499cb92021-12-02T19:47:38ZMagnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>10.1128/mSystems.00315-192379-5077https://doaj.org/article/bb5ed295422744fa891fbf8ca6499cb92019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00315-19https://doaj.org/toc/2379-5077ABSTRACT The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. IMPORTANCE A diversity of organisms can sense the geomagnetic field for the purpose of navigation. Magnetotactic bacteria are the most primitive magnetism-sensing organisms known thus far and represent an excellent model system for the study of the origin, evolution, and mechanism of microbial magnetoreception (or magnetotaxis). The present study is the first report focused on magnetosome gene cluster duplication in the Alphaproteobacteria, which suggests the important role of gene duplication in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. A novel scenario for the evolution of magnetotaxis in the Alphaproteobacteria is proposed and may provide new insights into evolution of magnetoreception of higher species.Haijian DuWenyan ZhangWensi ZhangWeijia ZhangHongmiao PanYongxin PanDennis A. BazylinskiLong-Fei WuTian XiaoWei LinAmerican Society for MicrobiologyarticleTerasakiellaevolutiongene duplicationgenomesmagnetosome gene clustermagnetotactic bacteriaMicrobiologyQR1-502ENmSystems, Vol 4, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Terasakiella evolution gene duplication genomes magnetosome gene cluster magnetotactic bacteria Microbiology QR1-502
spellingShingle	Terasakiella evolution gene duplication genomes magnetosome gene cluster magnetotactic bacteria Microbiology QR1-502 Haijian Du Wenyan Zhang Wensi Zhang Weijia Zhang Hongmiao Pan Yongxin Pan Dennis A. Bazylinski Long-Fei Wu Tian Xiao Wei Lin Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>
description	ABSTRACT The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. IMPORTANCE A diversity of organisms can sense the geomagnetic field for the purpose of navigation. Magnetotactic bacteria are the most primitive magnetism-sensing organisms known thus far and represent an excellent model system for the study of the origin, evolution, and mechanism of microbial magnetoreception (or magnetotaxis). The present study is the first report focused on magnetosome gene cluster duplication in the Alphaproteobacteria, which suggests the important role of gene duplication in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria. A novel scenario for the evolution of magnetotaxis in the Alphaproteobacteria is proposed and may provide new insights into evolution of magnetoreception of higher species.
format	article
author	Haijian Du Wenyan Zhang Wensi Zhang Weijia Zhang Hongmiao Pan Yongxin Pan Dennis A. Bazylinski Long-Fei Wu Tian Xiao Wei Lin
author_facet	Haijian Du Wenyan Zhang Wensi Zhang Weijia Zhang Hongmiao Pan Yongxin Pan Dennis A. Bazylinski Long-Fei Wu Tian Xiao Wei Lin
author_sort	Haijian Du
title	Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>
title_short	Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>
title_full	Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>
title_fullStr	Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>
title_full_unstemmed	Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>
title_sort	magnetosome gene duplication as an important driver in the evolution of magnetotaxis in the <italic toggle="yes">alphaproteobacteria</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/bb5ed295422744fa891fbf8ca6499cb9
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Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the <italic toggle="yes">Alphaproteobacteria</italic>

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