The evolution of bacterial mechanosensitive channels

Ian R. Booth; Samantha Miller; Axel Mueller; Laura Lehtovirta-Morley

doi:10.1016/j.ceca.2014.12.011

The evolution of bacterial mechanosensitive channels

Ian R. Booth^*, Samantha Miller, Axel Mueller, Laura Lehtovirta-Morley

^*Corresponding author for this work

Medical Sciences

Research output: Contribution to journal › Literature review › peer-review

32 Citations (Scopus)

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Abstract

Mechanosensitive channels are ubiquitous and highly studied. However, the evolution of the bacterial channels remains enigmatic. It can be argued that mechanosensitivity might be a feature of all membrane proteins with some becoming progressively less sensitive to membrane tension over the course of evolution. Bacteria and archaea exhibit two main classes of channels, MscS and MscL. Present day channels suggest that the evolution of MscL may be highly constrained, whereas MscS has undergone elaboration via gene fusion (and potentially gene fission) events to generate a diversity of channel structures. Some of these channel variants are constrained to a small number of genera or species. Some are only found in higher organisms. Only exceptionally have these diverse channels been investigated in any detail. In this review we consider both the processes that might have led to the evolved complexity but also some of the methods exploiting the explosion of genome sequences to understand (and/or track) their distribution. The role of MscS-related channels in calcium-mediated cell biology events is considered. (C) 2015 The Authors. Published by Elsevier Ltd.

Original language	English
Pages (from-to)	140-150
Number of pages	11
Journal	Cell Calcium
Volume	57
Issue number	3
Early online date	25 Dec 2014
DOIs	https://doi.org/10.1016/j.ceca.2014.12.011
Publication status	Published - Mar 2015

Bibliographical note

Acknowledgements
IRB is funded by a Leverhulme Emeritus Research Fellowship and a CEMI research grant from Caltech. IRB and SM are funded by a WT Programme Grant (092552/A/10/Z). LL is funded by a NERC grant to Professors J.I. Prosser and G. Nicol (NE/I027835/1). AM is funded by a NIH Director's Pioneer Award (Grant 1DP1OD008304-01) to Bill Clemons (Caltech). The authors wish to thank Suzi Black, Jessica Ricci, Cai Neubauer, Megan Bergkessel, Dianne Newman, Rob Phillips, Doug Rees and Bill Clemons and other members of the Miller, Newman, Naismith and Conway labs for their stimulating conversations. IRB, SM and LL would like to thank Jim Prosser and Graeme Nicol (University of Aberdeen) for encouraging LL to take part in this project and Bill Clemons (Caltech) for the participation of AM.

Keywords

mechanosensitive channels
MscS
MscL
gene synteny
potassium channels
ammonia-oxidizing archaeon
gated sodium-channel
escherichia-coli MSCS
Francisco Bay Estuary
draft genome sequence
of-function mutations
crystal-structure
bacillus-subtilis
osmotic downshock
potassium channel

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10.1016/j.ceca.2014.12.011Licence: CC BY-NC-ND

The evolution of bacterial mechanosensitive channels
© 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Final published version, 2 MBLicence: CC BY-NC-ND

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Cite this

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title = "The evolution of bacterial mechanosensitive channels",

abstract = "Mechanosensitive channels are ubiquitous and highly studied. However, the evolution of the bacterial channels remains enigmatic. It can be argued that mechanosensitivity might be a feature of all membrane proteins with some becoming progressively less sensitive to membrane tension over the course of evolution. Bacteria and archaea exhibit two main classes of channels, MscS and MscL. Present day channels suggest that the evolution of MscL may be highly constrained, whereas MscS has undergone elaboration via gene fusion (and potentially gene fission) events to generate a diversity of channel structures. Some of these channel variants are constrained to a small number of genera or species. Some are only found in higher organisms. Only exceptionally have these diverse channels been investigated in any detail. In this review we consider both the processes that might have led to the evolved complexity but also some of the methods exploiting the explosion of genome sequences to understand (and/or track) their distribution. The role of MscS-related channels in calcium-mediated cell biology events is considered. (C) 2015 The Authors. Published by Elsevier Ltd.",

keywords = "mechanosensitive channels, MscS, MscL, gene synteny, potassium channels, ammonia-oxidizing archaeon, gated sodium-channel, escherichia-coli MSCS, Francisco Bay Estuary, draft genome sequence, of-function mutations, crystal-structure, bacillus-subtilis, osmotic downshock, potassium channel",

author = "Booth, {Ian R.} and Samantha Miller and Axel Mueller and Laura Lehtovirta-Morley",

note = "Acknowledgements IRB is funded by a Leverhulme Emeritus Research Fellowship and a CEMI research grant from Caltech. IRB and SM are funded by a WT Programme Grant (092552/A/10/Z). LL is funded by a NERC grant to Professors J.I. Prosser and G. Nicol (NE/I027835/1). AM is funded by a NIH Director's Pioneer Award (Grant 1DP1OD008304-01) to Bill Clemons (Caltech). The authors wish to thank Suzi Black, Jessica Ricci, Cai Neubauer, Megan Bergkessel, Dianne Newman, Rob Phillips, Doug Rees and Bill Clemons and other members of the Miller, Newman, Naismith and Conway labs for their stimulating conversations. IRB, SM and LL would like to thank Jim Prosser and Graeme Nicol (University of Aberdeen) for encouraging LL to take part in this project and Bill Clemons (Caltech) for the participation of AM.",

year = "2015",

month = mar,

doi = "10.1016/j.ceca.2014.12.011",

language = "English",

volume = "57",

pages = "140--150",

journal = "Cell Calcium",

issn = "0143-4160",

publisher = "Churchill Livingstone",

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TY - JOUR

T1 - The evolution of bacterial mechanosensitive channels

AU - Booth, Ian R.

AU - Miller, Samantha

AU - Mueller, Axel

AU - Lehtovirta-Morley, Laura

N1 - Acknowledgements IRB is funded by a Leverhulme Emeritus Research Fellowship and a CEMI research grant from Caltech. IRB and SM are funded by a WT Programme Grant (092552/A/10/Z). LL is funded by a NERC grant to Professors J.I. Prosser and G. Nicol (NE/I027835/1). AM is funded by a NIH Director's Pioneer Award (Grant 1DP1OD008304-01) to Bill Clemons (Caltech). The authors wish to thank Suzi Black, Jessica Ricci, Cai Neubauer, Megan Bergkessel, Dianne Newman, Rob Phillips, Doug Rees and Bill Clemons and other members of the Miller, Newman, Naismith and Conway labs for their stimulating conversations. IRB, SM and LL would like to thank Jim Prosser and Graeme Nicol (University of Aberdeen) for encouraging LL to take part in this project and Bill Clemons (Caltech) for the participation of AM.

PY - 2015/3

Y1 - 2015/3

N2 - Mechanosensitive channels are ubiquitous and highly studied. However, the evolution of the bacterial channels remains enigmatic. It can be argued that mechanosensitivity might be a feature of all membrane proteins with some becoming progressively less sensitive to membrane tension over the course of evolution. Bacteria and archaea exhibit two main classes of channels, MscS and MscL. Present day channels suggest that the evolution of MscL may be highly constrained, whereas MscS has undergone elaboration via gene fusion (and potentially gene fission) events to generate a diversity of channel structures. Some of these channel variants are constrained to a small number of genera or species. Some are only found in higher organisms. Only exceptionally have these diverse channels been investigated in any detail. In this review we consider both the processes that might have led to the evolved complexity but also some of the methods exploiting the explosion of genome sequences to understand (and/or track) their distribution. The role of MscS-related channels in calcium-mediated cell biology events is considered. (C) 2015 The Authors. Published by Elsevier Ltd.

AB - Mechanosensitive channels are ubiquitous and highly studied. However, the evolution of the bacterial channels remains enigmatic. It can be argued that mechanosensitivity might be a feature of all membrane proteins with some becoming progressively less sensitive to membrane tension over the course of evolution. Bacteria and archaea exhibit two main classes of channels, MscS and MscL. Present day channels suggest that the evolution of MscL may be highly constrained, whereas MscS has undergone elaboration via gene fusion (and potentially gene fission) events to generate a diversity of channel structures. Some of these channel variants are constrained to a small number of genera or species. Some are only found in higher organisms. Only exceptionally have these diverse channels been investigated in any detail. In this review we consider both the processes that might have led to the evolved complexity but also some of the methods exploiting the explosion of genome sequences to understand (and/or track) their distribution. The role of MscS-related channels in calcium-mediated cell biology events is considered. (C) 2015 The Authors. Published by Elsevier Ltd.

KW - mechanosensitive channels

KW - MscS

KW - MscL

KW - gene synteny

KW - potassium channels

KW - ammonia-oxidizing archaeon

KW - gated sodium-channel

KW - escherichia-coli MSCS

KW - Francisco Bay Estuary

KW - draft genome sequence

KW - of-function mutations

KW - crystal-structure

KW - bacillus-subtilis

KW - osmotic downshock

KW - potassium channel

U2 - 10.1016/j.ceca.2014.12.011

DO - 10.1016/j.ceca.2014.12.011

M3 - Literature review

SN - 0143-4160

VL - 57

SP - 140

EP - 150

JO - Cell Calcium

JF - Cell Calcium

IS - 3

ER -

The evolution of bacterial mechanosensitive channels

Abstract

Bibliographical note

Keywords

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