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Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism

During evolution, enzymes can undergo shifts in preferred substrates or in catalytic activities. An intriguing question is how enzyme function changes following horizontal gene transfer, especially for bacterial genes that have moved to animal genomes. Some insects have acquired genes that encode en...

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Autores principales: Smith, Thomas E., Lee, Mijoon, Person, Maria D., Hesek, Dusan, Mobashery, Shahriar, Moran, Nancy A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8689515/
https://www.ncbi.nlm.nih.gov/pubmed/34933456
http://dx.doi.org/10.1128/mBio.02636-21
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author Smith, Thomas E.
Lee, Mijoon
Person, Maria D.
Hesek, Dusan
Mobashery, Shahriar
Moran, Nancy A.
author_facet Smith, Thomas E.
Lee, Mijoon
Person, Maria D.
Hesek, Dusan
Mobashery, Shahriar
Moran, Nancy A.
author_sort Smith, Thomas E.
collection PubMed
description During evolution, enzymes can undergo shifts in preferred substrates or in catalytic activities. An intriguing question is how enzyme function changes following horizontal gene transfer, especially for bacterial genes that have moved to animal genomes. Some insects have acquired genes that encode enzymes for the biosynthesis of bacterial cell wall components and that appear to function to support or control their obligate endosymbiotic bacteria. In aphids, the bacterial endosymbiont Buchnera aphidicola provides essential amino acids for aphid hosts but lacks most genes for remodeling of the bacterial cell wall. The aphid genome has acquired seven genes with putative functions in cell wall metabolism that are primarily expressed in the aphid cells harboring Buchnera. In analyses of aphid homogenates, we detected peptidoglycan (PGN) muropeptides indicative of the reactions of PGN hydrolases encoded by horizontally acquired aphid genes but not by Buchnera genes. We produced one such host enzyme, ApLdcA, and characterized its activity with both cell wall derived and synthetic PGN. Both ApLdcA and the homologous enzyme in Escherichia coli, which functions as an l,d-carboxypeptidase in the cytoplasmic PGN recycling pathway, exhibit turnover of PGN substrates containing stem pentapeptides and cross-linkages via l,d-endopeptidase activity, consistent with a potential role in cell wall remodeling. Our results suggest that ApLdcA derives its functions from the promiscuous activities of an ancestral LdcA enzyme, whose acquisition by the aphid genome may have enabled hosts to influence Buchnera cell wall metabolism as a means to control symbiont growth and division.
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spelling pubmed-86895152021-12-27 Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism Smith, Thomas E. Lee, Mijoon Person, Maria D. Hesek, Dusan Mobashery, Shahriar Moran, Nancy A. mBio Research Article During evolution, enzymes can undergo shifts in preferred substrates or in catalytic activities. An intriguing question is how enzyme function changes following horizontal gene transfer, especially for bacterial genes that have moved to animal genomes. Some insects have acquired genes that encode enzymes for the biosynthesis of bacterial cell wall components and that appear to function to support or control their obligate endosymbiotic bacteria. In aphids, the bacterial endosymbiont Buchnera aphidicola provides essential amino acids for aphid hosts but lacks most genes for remodeling of the bacterial cell wall. The aphid genome has acquired seven genes with putative functions in cell wall metabolism that are primarily expressed in the aphid cells harboring Buchnera. In analyses of aphid homogenates, we detected peptidoglycan (PGN) muropeptides indicative of the reactions of PGN hydrolases encoded by horizontally acquired aphid genes but not by Buchnera genes. We produced one such host enzyme, ApLdcA, and characterized its activity with both cell wall derived and synthetic PGN. Both ApLdcA and the homologous enzyme in Escherichia coli, which functions as an l,d-carboxypeptidase in the cytoplasmic PGN recycling pathway, exhibit turnover of PGN substrates containing stem pentapeptides and cross-linkages via l,d-endopeptidase activity, consistent with a potential role in cell wall remodeling. Our results suggest that ApLdcA derives its functions from the promiscuous activities of an ancestral LdcA enzyme, whose acquisition by the aphid genome may have enabled hosts to influence Buchnera cell wall metabolism as a means to control symbiont growth and division. American Society for Microbiology 2021-12-21 /pmc/articles/PMC8689515/ /pubmed/34933456 http://dx.doi.org/10.1128/mBio.02636-21 Text en Copyright © 2021 Smith et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Smith, Thomas E.
Lee, Mijoon
Person, Maria D.
Hesek, Dusan
Mobashery, Shahriar
Moran, Nancy A.
Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism
title Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism
title_full Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism
title_fullStr Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism
title_full_unstemmed Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism
title_short Horizontal-Acquisition of a Promiscuous Peptidoglycan-Recycling Enzyme Enables Aphids To Influence Symbiont Cell Wall Metabolism
title_sort horizontal-acquisition of a promiscuous peptidoglycan-recycling enzyme enables aphids to influence symbiont cell wall metabolism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8689515/
https://www.ncbi.nlm.nih.gov/pubmed/34933456
http://dx.doi.org/10.1128/mBio.02636-21
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