Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli

Genes encoding the photoreactive protein proteorhodopsin (PR) have been found in a wide range of marine bacterial species, reflecting the significant contribution that PR makes to energy flux and carbon cycling in ocean ecosystems. PR can also confer advantages to enhance the ability of the marine b...

Descrizione completa

Dettagli Bibliografici
Autori principali: Song, Y, Cartron, M, Jackson, P, Davison, P, Dickman, M, Zhu, D, Huang, W, Hunter, C
Natura: Journal article
Pubblicazione: American Society for Microbiology 2019
_version_ 1826298116339400704
author Song, Y
Cartron, M
Jackson, P
Davison, P
Dickman, M
Zhu, D
Huang, W
Hunter, C
author_facet Song, Y
Cartron, M
Jackson, P
Davison, P
Dickman, M
Zhu, D
Huang, W
Hunter, C
author_sort Song, Y
collection OXFORD
description Genes encoding the photoreactive protein proteorhodopsin (PR) have been found in a wide range of marine bacterial species, reflecting the significant contribution that PR makes to energy flux and carbon cycling in ocean ecosystems. PR can also confer advantages to enhance the ability of the marine bacteria to survive periods of starvation. Here, we investigate the effect of heterologously produced PR on the viability of Escherichia coli. Quantitative mass spectrometry shows that E. coli, exogenously supplied with the retinal cofactor, assembles as many as 187,000 holo-PR molecules per cell, accounting for approximately 47% of the membrane area; even cells with no retinal synthesise ∼148,000 apo-PR molecules per cell. We show that populations of E. coli cells containing PR exhibit significantly extended viability over many weeks and we use single cell Raman spectroscopy (SCRS) to detect holo-PR in nine-month old cells. SCRS shows that such cells, even incubated in the dark and therefore with inactive PR, maintain cellular levels of DNA and RNA and avoid deterioration of the cytoplasmic membrane, a likely basis for extended viability. The substantial proportion of the E. coli membrane required to accommodate high levels of PR likely fosters extensive intermolecular contacts, suggested to physically stabilise the cell membrane and impart a long-term benefit manifested as extended viability in the dark. We propose that marine bacteria could benefit similarly from a high PR content, with a stabilised cell membrane extending the survival when those bacteria experience periods of severe nutrient or light limitation in the oceans.
first_indexed 2024-03-07T04:41:56Z
format Journal article
id oxford-uuid:d1efdbeb-3363-4f6d-a699-133c94fa5327
institution University of Oxford
last_indexed 2024-03-07T04:41:56Z
publishDate 2019
publisher American Society for Microbiology
record_format dspace
spelling oxford-uuid:d1efdbeb-3363-4f6d-a699-133c94fa53272022-03-27T08:00:29ZOverproduction of proteorhodopsin enhances long-term viability of Escherichia coliJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:d1efdbeb-3363-4f6d-a699-133c94fa5327Symplectic Elements at OxfordAmerican Society for Microbiology2019Song, YCartron, MJackson, PDavison, PDickman, MZhu, DHuang, WHunter, CGenes encoding the photoreactive protein proteorhodopsin (PR) have been found in a wide range of marine bacterial species, reflecting the significant contribution that PR makes to energy flux and carbon cycling in ocean ecosystems. PR can also confer advantages to enhance the ability of the marine bacteria to survive periods of starvation. Here, we investigate the effect of heterologously produced PR on the viability of Escherichia coli. Quantitative mass spectrometry shows that E. coli, exogenously supplied with the retinal cofactor, assembles as many as 187,000 holo-PR molecules per cell, accounting for approximately 47% of the membrane area; even cells with no retinal synthesise ∼148,000 apo-PR molecules per cell. We show that populations of E. coli cells containing PR exhibit significantly extended viability over many weeks and we use single cell Raman spectroscopy (SCRS) to detect holo-PR in nine-month old cells. SCRS shows that such cells, even incubated in the dark and therefore with inactive PR, maintain cellular levels of DNA and RNA and avoid deterioration of the cytoplasmic membrane, a likely basis for extended viability. The substantial proportion of the E. coli membrane required to accommodate high levels of PR likely fosters extensive intermolecular contacts, suggested to physically stabilise the cell membrane and impart a long-term benefit manifested as extended viability in the dark. We propose that marine bacteria could benefit similarly from a high PR content, with a stabilised cell membrane extending the survival when those bacteria experience periods of severe nutrient or light limitation in the oceans.
spellingShingle Song, Y
Cartron, M
Jackson, P
Davison, P
Dickman, M
Zhu, D
Huang, W
Hunter, C
Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli
title Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli
title_full Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli
title_fullStr Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli
title_full_unstemmed Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli
title_short Overproduction of proteorhodopsin enhances long-term viability of Escherichia coli
title_sort overproduction of proteorhodopsin enhances long term viability of escherichia coli
work_keys_str_mv AT songy overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT cartronm overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT jacksonp overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT davisonp overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT dickmanm overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT zhud overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT huangw overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli
AT hunterc overproductionofproteorhodopsinenhanceslongtermviabilityofescherichiacoli