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Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila

Previous work has shown that the obligate intracellular amoebal endosymbiont Neochlamydia S13, an environmental chlamydia strain, has an amoebal infection rate of 100%, but does not cause amoebal lysis and lacks transferability to other host amoebae. The underlying mechanism for these observations r...

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Autores principales: Ishida, Kasumi, Sekizuka, Tsuyoshi, Hayashida, Kyoko, Matsuo, Junji, Takeuchi, Fumihiko, Kuroda, Makoto, Nakamura, Shinji, Yamazaki, Tomohiro, Yoshida, Mitsutaka, Takahashi, Kaori, Nagai, Hiroki, Sugimoto, Chihiro, Yamaguchi, Hiroyuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3991601/
https://www.ncbi.nlm.nih.gov/pubmed/24747986
http://dx.doi.org/10.1371/journal.pone.0095166
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author Ishida, Kasumi
Sekizuka, Tsuyoshi
Hayashida, Kyoko
Matsuo, Junji
Takeuchi, Fumihiko
Kuroda, Makoto
Nakamura, Shinji
Yamazaki, Tomohiro
Yoshida, Mitsutaka
Takahashi, Kaori
Nagai, Hiroki
Sugimoto, Chihiro
Yamaguchi, Hiroyuki
author_facet Ishida, Kasumi
Sekizuka, Tsuyoshi
Hayashida, Kyoko
Matsuo, Junji
Takeuchi, Fumihiko
Kuroda, Makoto
Nakamura, Shinji
Yamazaki, Tomohiro
Yoshida, Mitsutaka
Takahashi, Kaori
Nagai, Hiroki
Sugimoto, Chihiro
Yamaguchi, Hiroyuki
author_sort Ishida, Kasumi
collection PubMed
description Previous work has shown that the obligate intracellular amoebal endosymbiont Neochlamydia S13, an environmental chlamydia strain, has an amoebal infection rate of 100%, but does not cause amoebal lysis and lacks transferability to other host amoebae. The underlying mechanism for these observations remains unknown. In this study, we found that the host amoeba could completely evade Legionella infection. The draft genome sequence of Neochlamydia S13 revealed several defects in essential metabolic pathways, as well as unique molecules with leucine-rich repeats (LRRs) and ankyrin domains, responsible for protein-protein interaction. Neochlamydia S13 lacked an intact tricarboxylic acid cycle and had an incomplete respiratory chain. ADP/ATP translocases, ATP-binding cassette transporters, and secretion systems (types II and III) were well conserved, but no type IV secretion system was found. The number of outer membrane proteins (OmcB, PomS, 76-kDa protein, and OmpW) was limited. Interestingly, genes predicting unique proteins with LRRs (30 genes) or ankyrin domains (one gene) were identified. Furthermore, 33 transposases were found, possibly explaining the drastic genome modification. Taken together, the genomic features of Neochlamydia S13 explain the intimate interaction with the host amoeba to compensate for bacterial metabolic defects, and illuminate the role of the endosymbiont in the defense of the host amoebae against Legionella infection.
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spelling pubmed-39916012014-04-21 Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila Ishida, Kasumi Sekizuka, Tsuyoshi Hayashida, Kyoko Matsuo, Junji Takeuchi, Fumihiko Kuroda, Makoto Nakamura, Shinji Yamazaki, Tomohiro Yoshida, Mitsutaka Takahashi, Kaori Nagai, Hiroki Sugimoto, Chihiro Yamaguchi, Hiroyuki PLoS One Research Article Previous work has shown that the obligate intracellular amoebal endosymbiont Neochlamydia S13, an environmental chlamydia strain, has an amoebal infection rate of 100%, but does not cause amoebal lysis and lacks transferability to other host amoebae. The underlying mechanism for these observations remains unknown. In this study, we found that the host amoeba could completely evade Legionella infection. The draft genome sequence of Neochlamydia S13 revealed several defects in essential metabolic pathways, as well as unique molecules with leucine-rich repeats (LRRs) and ankyrin domains, responsible for protein-protein interaction. Neochlamydia S13 lacked an intact tricarboxylic acid cycle and had an incomplete respiratory chain. ADP/ATP translocases, ATP-binding cassette transporters, and secretion systems (types II and III) were well conserved, but no type IV secretion system was found. The number of outer membrane proteins (OmcB, PomS, 76-kDa protein, and OmpW) was limited. Interestingly, genes predicting unique proteins with LRRs (30 genes) or ankyrin domains (one gene) were identified. Furthermore, 33 transposases were found, possibly explaining the drastic genome modification. Taken together, the genomic features of Neochlamydia S13 explain the intimate interaction with the host amoeba to compensate for bacterial metabolic defects, and illuminate the role of the endosymbiont in the defense of the host amoebae against Legionella infection. Public Library of Science 2014-04-18 /pmc/articles/PMC3991601/ /pubmed/24747986 http://dx.doi.org/10.1371/journal.pone.0095166 Text en © 2014 Ishida et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Ishida, Kasumi
Sekizuka, Tsuyoshi
Hayashida, Kyoko
Matsuo, Junji
Takeuchi, Fumihiko
Kuroda, Makoto
Nakamura, Shinji
Yamazaki, Tomohiro
Yoshida, Mitsutaka
Takahashi, Kaori
Nagai, Hiroki
Sugimoto, Chihiro
Yamaguchi, Hiroyuki
Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila
title Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila
title_full Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila
title_fullStr Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila
title_full_unstemmed Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila
title_short Amoebal Endosymbiont Neochlamydia Genome Sequence Illuminates the Bacterial Role in the Defense of the Host Amoebae against Legionella pneumophila
title_sort amoebal endosymbiont neochlamydia genome sequence illuminates the bacterial role in the defense of the host amoebae against legionella pneumophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3991601/
https://www.ncbi.nlm.nih.gov/pubmed/24747986
http://dx.doi.org/10.1371/journal.pone.0095166
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