Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary

ABSTRACT Halobacteriovorax strains are saltwater-adapted predatory bacteria that attack Gram-negative bacteria and may play an important role in shaping microbial communities. To understand how Halobacteriovorax strains impact ecosystems and develop them as biocontrol agents, it is important to char...

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Autores principales: Brett G. Enos, Molly K. Anthony, Joseph A. DeGiorgis, Laura E. Williams
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:1136292e801445d2aceed650a860cb0d2021-11-15T15:22:02ZPrey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary10.1128/mSphere.00508-172379-5042https://doaj.org/article/1136292e801445d2aceed650a860cb0d2018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00508-17https://doaj.org/toc/2379-5042ABSTRACT Halobacteriovorax strains are saltwater-adapted predatory bacteria that attack Gram-negative bacteria and may play an important role in shaping microbial communities. To understand how Halobacteriovorax strains impact ecosystems and develop them as biocontrol agents, it is important to characterize variation in predation phenotypes and investigate Halobacteriovorax genome evolution. We isolated Halobacteriovorax marinus BE01 from an estuary in Rhode Island using Vibrio from the same site as prey. Small, fast-moving, attack-phase BE01 cells attach to and invade prey cells, consistent with the intraperiplasmic predation strategy of the H. marinus type strain, SJ. BE01 is a prey generalist, forming plaques on Vibrio strains from the estuary, Pseudomonas from soil, and Escherichia coli. Genome analysis revealed extremely high conservation of gene order and amino acid sequences between BE01 and SJ, suggesting strong selective pressure to maintain the genome in this H. marinus lineage. Despite this, we identified two regions of gene content difference that likely resulted from horizontal gene transfer. Analysis of modal codon usage frequencies supports the hypothesis that these regions were acquired from bacteria with different codon usage biases than H. marinus. In one of these regions, BE01 and SJ carry different genes associated with mobile genetic elements. Acquired functions in BE01 include the dnd operon, which encodes a pathway for DNA modification, and a suite of genes involved in membrane synthesis and regulation of gene expression that was likely acquired from another Halobacteriovorax lineage. This analysis provides further evidence that horizontal gene transfer plays an important role in genome evolution in predatory bacteria. IMPORTANCE Predatory bacteria attack and digest other bacteria and therefore may play a role in shaping microbial communities. To investigate phenotypic and genotypic variation in saltwater-adapted predatory bacteria, we isolated Halobacteriovorax marinus BE01 from an estuary in Rhode Island, assayed whether it could attack different prey bacteria, and sequenced and analyzed its genome. We found that BE01 is a prey generalist, attacking bacteria from different phylogenetic groups and environments. Gene order and amino acid sequences are highly conserved between BE01 and the H. marinus type strain, SJ. By comparative genomics, we detected two regions of gene content difference that likely occurred via horizontal gene transfer events. Acquired genes encode functions such as modification of DNA, membrane synthesis and regulation of gene expression. Understanding genome evolution and variation in predation phenotypes among predatory bacteria will inform their development as biocontrol agents and clarify how they impact microbial communities.Brett G. EnosMolly K. AnthonyJoseph A. DeGiorgisLaura E. WilliamsAmerican Society for Microbiologyarticlehorizontal gene transferhost rangemarine ecosystemmobile genetic elementpredationMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution DOAJ
collection DOAJ
language EN
topic horizontal gene transfer
host range
marine ecosystem
mobile genetic element
predation
Microbiology
QR1-502
spellingShingle horizontal gene transfer
host range
marine ecosystem
mobile genetic element
predation
Microbiology
QR1-502
Brett G. Enos
Molly K. Anthony
Joseph A. DeGiorgis
Laura E. Williams
Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary
description ABSTRACT Halobacteriovorax strains are saltwater-adapted predatory bacteria that attack Gram-negative bacteria and may play an important role in shaping microbial communities. To understand how Halobacteriovorax strains impact ecosystems and develop them as biocontrol agents, it is important to characterize variation in predation phenotypes and investigate Halobacteriovorax genome evolution. We isolated Halobacteriovorax marinus BE01 from an estuary in Rhode Island using Vibrio from the same site as prey. Small, fast-moving, attack-phase BE01 cells attach to and invade prey cells, consistent with the intraperiplasmic predation strategy of the H. marinus type strain, SJ. BE01 is a prey generalist, forming plaques on Vibrio strains from the estuary, Pseudomonas from soil, and Escherichia coli. Genome analysis revealed extremely high conservation of gene order and amino acid sequences between BE01 and SJ, suggesting strong selective pressure to maintain the genome in this H. marinus lineage. Despite this, we identified two regions of gene content difference that likely resulted from horizontal gene transfer. Analysis of modal codon usage frequencies supports the hypothesis that these regions were acquired from bacteria with different codon usage biases than H. marinus. In one of these regions, BE01 and SJ carry different genes associated with mobile genetic elements. Acquired functions in BE01 include the dnd operon, which encodes a pathway for DNA modification, and a suite of genes involved in membrane synthesis and regulation of gene expression that was likely acquired from another Halobacteriovorax lineage. This analysis provides further evidence that horizontal gene transfer plays an important role in genome evolution in predatory bacteria. IMPORTANCE Predatory bacteria attack and digest other bacteria and therefore may play a role in shaping microbial communities. To investigate phenotypic and genotypic variation in saltwater-adapted predatory bacteria, we isolated Halobacteriovorax marinus BE01 from an estuary in Rhode Island, assayed whether it could attack different prey bacteria, and sequenced and analyzed its genome. We found that BE01 is a prey generalist, attacking bacteria from different phylogenetic groups and environments. Gene order and amino acid sequences are highly conserved between BE01 and the H. marinus type strain, SJ. By comparative genomics, we detected two regions of gene content difference that likely occurred via horizontal gene transfer events. Acquired genes encode functions such as modification of DNA, membrane synthesis and regulation of gene expression. Understanding genome evolution and variation in predation phenotypes among predatory bacteria will inform their development as biocontrol agents and clarify how they impact microbial communities.
format article
author Brett G. Enos
Molly K. Anthony
Joseph A. DeGiorgis
Laura E. Williams
author_facet Brett G. Enos
Molly K. Anthony
Joseph A. DeGiorgis
Laura E. Williams
author_sort Brett G. Enos
title Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary
title_short Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary
title_full Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary
title_fullStr Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary
title_full_unstemmed Prey Range and Genome Evolution of <named-content content-type="genus-species">Halobacteriovorax marinus</named-content> Predatory Bacteria from an Estuary
title_sort prey range and genome evolution of <named-content content-type="genus-species">halobacteriovorax marinus</named-content> predatory bacteria from an estuary
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/1136292e801445d2aceed650a860cb0d
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