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Natural History and Ecology of Interactions Between Bordetella Species and Amoeba

A variety of bacteria have evolved the ability to interact with environmental phagocytic predators such as amoebae, which may have facilitated their subsequent interactions with phagocytes in animal hosts. Our recent study found that the animal pathogen Bordetella bronchiseptica can evade predation...

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Autores principales: Ma, Longhuan, Linz, Bodo, Caulfield, Amanda D., Dewan, Kalyan K., Rivera, Israel, Harvill, Eric T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8863592/
https://www.ncbi.nlm.nih.gov/pubmed/35223538
http://dx.doi.org/10.3389/fcimb.2022.798317
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author Ma, Longhuan
Linz, Bodo
Caulfield, Amanda D.
Dewan, Kalyan K.
Rivera, Israel
Harvill, Eric T.
author_facet Ma, Longhuan
Linz, Bodo
Caulfield, Amanda D.
Dewan, Kalyan K.
Rivera, Israel
Harvill, Eric T.
author_sort Ma, Longhuan
collection PubMed
description A variety of bacteria have evolved the ability to interact with environmental phagocytic predators such as amoebae, which may have facilitated their subsequent interactions with phagocytes in animal hosts. Our recent study found that the animal pathogen Bordetella bronchiseptica can evade predation by the common soil amoeba Dictyostelium discoideum, survive within, and hijack its complex life cycle as a propagation and dissemination vector. However, it is uncertain whether the mechanisms allowing interactions with predatory amoebae are conserved among Bordetella species, because divergence, evolution, and adaptation to different hosts and ecological niches was accompanied by acquisition and loss of many genes. Here we tested 9 diverse Bordetella species in three assays representing distinct aspects of their interactions with D. discoideum. Several human and animal pathogens retained the abilities to survive within single-celled amoeba, to inhibit amoebic plaque expansion, and to translocate with amoebae to the fruiting body and disseminate along with the fruiting body. In contrast, these abilities were partly degraded for the bird pathogen B. avium, and for the human-restricted species B. pertussis and B. parapertussis. Interestingly, a different lineage of B. parapertussis only known to infect sheep retained the ability to interact with D. discoideum, demonstrating that these abilities were lost in multiple lineages independently, correlating with niche specialization and recent rapid genome decay apparently mediated by insertion sequences. B. petrii has been isolated sporadically from diverse human and environmental sources, has acquired insertion sequences, undergone genome decay and has also lost the ability to interact with amoebae, suggesting some specialization to some unknown niche. A genome-wide association study (GWAS) identified a set of genes that are potentially associated with the ability to interact with D. discoideum. These results suggest that massive gene loss associated with specialization of some Bordetella species to a closed life cycle in a particular host was repeatedly and independently accompanied by loss of the ability to interact with amoebae in an environmental niche.
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spelling pubmed-88635922022-02-24 Natural History and Ecology of Interactions Between Bordetella Species and Amoeba Ma, Longhuan Linz, Bodo Caulfield, Amanda D. Dewan, Kalyan K. Rivera, Israel Harvill, Eric T. Front Cell Infect Microbiol Cellular and Infection Microbiology A variety of bacteria have evolved the ability to interact with environmental phagocytic predators such as amoebae, which may have facilitated their subsequent interactions with phagocytes in animal hosts. Our recent study found that the animal pathogen Bordetella bronchiseptica can evade predation by the common soil amoeba Dictyostelium discoideum, survive within, and hijack its complex life cycle as a propagation and dissemination vector. However, it is uncertain whether the mechanisms allowing interactions with predatory amoebae are conserved among Bordetella species, because divergence, evolution, and adaptation to different hosts and ecological niches was accompanied by acquisition and loss of many genes. Here we tested 9 diverse Bordetella species in three assays representing distinct aspects of their interactions with D. discoideum. Several human and animal pathogens retained the abilities to survive within single-celled amoeba, to inhibit amoebic plaque expansion, and to translocate with amoebae to the fruiting body and disseminate along with the fruiting body. In contrast, these abilities were partly degraded for the bird pathogen B. avium, and for the human-restricted species B. pertussis and B. parapertussis. Interestingly, a different lineage of B. parapertussis only known to infect sheep retained the ability to interact with D. discoideum, demonstrating that these abilities were lost in multiple lineages independently, correlating with niche specialization and recent rapid genome decay apparently mediated by insertion sequences. B. petrii has been isolated sporadically from diverse human and environmental sources, has acquired insertion sequences, undergone genome decay and has also lost the ability to interact with amoebae, suggesting some specialization to some unknown niche. A genome-wide association study (GWAS) identified a set of genes that are potentially associated with the ability to interact with D. discoideum. These results suggest that massive gene loss associated with specialization of some Bordetella species to a closed life cycle in a particular host was repeatedly and independently accompanied by loss of the ability to interact with amoebae in an environmental niche. Frontiers Media S.A. 2022-02-09 /pmc/articles/PMC8863592/ /pubmed/35223538 http://dx.doi.org/10.3389/fcimb.2022.798317 Text en Copyright © 2022 Ma, Linz, Caulfield, Dewan, Rivera and Harvill https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Ma, Longhuan
Linz, Bodo
Caulfield, Amanda D.
Dewan, Kalyan K.
Rivera, Israel
Harvill, Eric T.
Natural History and Ecology of Interactions Between Bordetella Species and Amoeba
title Natural History and Ecology of Interactions Between Bordetella Species and Amoeba
title_full Natural History and Ecology of Interactions Between Bordetella Species and Amoeba
title_fullStr Natural History and Ecology of Interactions Between Bordetella Species and Amoeba
title_full_unstemmed Natural History and Ecology of Interactions Between Bordetella Species and Amoeba
title_short Natural History and Ecology of Interactions Between Bordetella Species and Amoeba
title_sort natural history and ecology of interactions between bordetella species and amoeba
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8863592/
https://www.ncbi.nlm.nih.gov/pubmed/35223538
http://dx.doi.org/10.3389/fcimb.2022.798317
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