AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17

ABSTRACT This study describes the functional characterization of two proteins, AupA and AupB, which are required for growth on alkanes in the marine hydrocarbonoclastic bacterium Marinobacter hydrocarbonoclasticus. The aupA and aupB genes form an operon whose expression was increased upon adhesion t...

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Autores principales: Julie Mounier, Florence Hakil, Priscilla Branchu, Muriel Naïtali, Philippe Goulas, Pierre Sivadon, Régis Grimaud
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:3d7554f18bf54b4486801f6f3309c52e2021-11-15T16:00:25ZAupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP1710.1128/mBio.00520-182150-7511https://doaj.org/article/3d7554f18bf54b4486801f6f3309c52e2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00520-18https://doaj.org/toc/2150-7511ABSTRACT This study describes the functional characterization of two proteins, AupA and AupB, which are required for growth on alkanes in the marine hydrocarbonoclastic bacterium Marinobacter hydrocarbonoclasticus. The aupA and aupB genes form an operon whose expression was increased upon adhesion to and biofilm formation on n-hexadecane. AupA and AupB are outer and inner membrane proteins, respectively, which are able to interact physically. Mutations in aupA or/and aupB reduced growth on solid paraffin and liquid n-hexadecane, while growth on nonalkane substrates was not affected. In contrast, growth of aup mutants on n-hexadecane solubilized in Brij 58 micelles was completely abolished. Mutant cells had also lost the ability to bind to n-hexadecane solubilized in Brij 58 micelles. These results support the involvement of AupA and AupB in the uptake of micelle-solubilized alkanes and provide the first evidence for a cellular process involved in the micellar uptake pathway. The phylogenetic distribution of the aupAB operon revealed that it is widespread in marine hydrocarbonoclastic bacteria of the orders Oceanospirillales and Alteromonadales and that it is present in high copy number (up to six) in some Alcanivorax strains. These features suggest that Aup proteins probably confer a selective advantage in alkane-contaminated seawater. IMPORTANCE Bacteria are the main actors of the biological removal of hydrocarbons in seawater, and so, it is important to understand how they degrade hydrocarbons and thereby mitigate marine environmental damage. Despite a considerable amount of literature about the dynamic of microbial communities subjected to hydrocarbon exposure and the isolation of strains that degrade hydrocarbons, most of the genetic determinants and molecular mechanisms of bacterial hydrocarbon uptake remain unknown. This study identifies two genes, aupA and aupB, in the hydrocarbonoclastic bacterium Marinobacter hydrocarbonoclasticus that are present frequently in multiple copies in most of the marine hydrocarbon-degrading bacteria for which the genomic sequence is available. AupA and AupB are two novel membrane proteins interacting together that are involved in the uptake of alkanes dissolved in surfactant micelles. The function and the phylogenetic distribution of aupA and aupB suggest that they might be one attribute of the remarkable adaptation of marine hydrocarbonoclastic bacteria that allow them to take advantage of hydrocarbons.Julie MounierFlorence HakilPriscilla BranchuMuriel NaïtaliPhilippe GoulasPierre SivadonRégis GrimaudAmerican Society for Microbiologyarticlealkanesbiodegradationbiofilmsmarine microbiologyMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic alkanes
biodegradation
biofilms
marine microbiology
Microbiology
QR1-502
spellingShingle alkanes
biodegradation
biofilms
marine microbiology
Microbiology
QR1-502
Julie Mounier
Florence Hakil
Priscilla Branchu
Muriel Naïtali
Philippe Goulas
Pierre Sivadon
Régis Grimaud
AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17
description ABSTRACT This study describes the functional characterization of two proteins, AupA and AupB, which are required for growth on alkanes in the marine hydrocarbonoclastic bacterium Marinobacter hydrocarbonoclasticus. The aupA and aupB genes form an operon whose expression was increased upon adhesion to and biofilm formation on n-hexadecane. AupA and AupB are outer and inner membrane proteins, respectively, which are able to interact physically. Mutations in aupA or/and aupB reduced growth on solid paraffin and liquid n-hexadecane, while growth on nonalkane substrates was not affected. In contrast, growth of aup mutants on n-hexadecane solubilized in Brij 58 micelles was completely abolished. Mutant cells had also lost the ability to bind to n-hexadecane solubilized in Brij 58 micelles. These results support the involvement of AupA and AupB in the uptake of micelle-solubilized alkanes and provide the first evidence for a cellular process involved in the micellar uptake pathway. The phylogenetic distribution of the aupAB operon revealed that it is widespread in marine hydrocarbonoclastic bacteria of the orders Oceanospirillales and Alteromonadales and that it is present in high copy number (up to six) in some Alcanivorax strains. These features suggest that Aup proteins probably confer a selective advantage in alkane-contaminated seawater. IMPORTANCE Bacteria are the main actors of the biological removal of hydrocarbons in seawater, and so, it is important to understand how they degrade hydrocarbons and thereby mitigate marine environmental damage. Despite a considerable amount of literature about the dynamic of microbial communities subjected to hydrocarbon exposure and the isolation of strains that degrade hydrocarbons, most of the genetic determinants and molecular mechanisms of bacterial hydrocarbon uptake remain unknown. This study identifies two genes, aupA and aupB, in the hydrocarbonoclastic bacterium Marinobacter hydrocarbonoclasticus that are present frequently in multiple copies in most of the marine hydrocarbon-degrading bacteria for which the genomic sequence is available. AupA and AupB are two novel membrane proteins interacting together that are involved in the uptake of alkanes dissolved in surfactant micelles. The function and the phylogenetic distribution of aupA and aupB suggest that they might be one attribute of the remarkable adaptation of marine hydrocarbonoclastic bacteria that allow them to take advantage of hydrocarbons.
format article
author Julie Mounier
Florence Hakil
Priscilla Branchu
Muriel Naïtali
Philippe Goulas
Pierre Sivadon
Régis Grimaud
author_facet Julie Mounier
Florence Hakil
Priscilla Branchu
Muriel Naïtali
Philippe Goulas
Pierre Sivadon
Régis Grimaud
author_sort Julie Mounier
title AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17
title_short AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17
title_full AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17
title_fullStr AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17
title_full_unstemmed AupA and AupB Are Outer and Inner Membrane Proteins Involved in Alkane Uptake in <named-content content-type="genus-species">Marinobacter hydrocarbonoclasticus</named-content> SP17
title_sort aupa and aupb are outer and inner membrane proteins involved in alkane uptake in <named-content content-type="genus-species">marinobacter hydrocarbonoclasticus</named-content> sp17
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/3d7554f18bf54b4486801f6f3309c52e
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