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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| Veröffentlicht in: | PloS one 2014-04, Vol.9 (4), p.e95166 |
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| creator | 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 |
| 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. |
| doi_str_mv | 10.1371/journal.pone.0095166 |
| format | Article |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0095166</identifier><identifier>PMID: 24747986</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adenosine diphosphate ; Amoeba ; Amoeba - pathogenicity ; Amoeba - physiology ; Anaplasma phagocytophilum ; Ankyrins ; ATP ; ATP-binding protein ; Bacteria ; Bacterial genetics ; Bioinformatics ; Biology and Life Sciences ; Chlamydia ; Chlamydia - genetics ; Chlamydia - pathogenicity ; Computer and Information Sciences ; Defects ; Electron transport ; Genes ; Genetic aspects ; Genome, Bacterial ; Genomes ; Genomics ; Health sciences ; Infections ; Infectious diseases ; Legionella ; Legionella pneumophila - pathogenicity ; Legionellosis ; Legionnaires' disease ; Legionnaires' disease bacterium ; Leucine ; Lysis ; Medical laboratories ; Medicine and Health Sciences ; Membrane proteins ; Metabolic pathways ; Molecular Sequence Data ; Nucleotide sequence ; Outer membrane proteins ; Phylogenetics ; Protein interaction ; Proteins ; Research and Analysis Methods ; Sexually transmitted diseases ; STD ; Symbiosis ; Tricarboxylic acid cycle ; University graduates ; Zoonoses</subject><ispartof>PloS one, 2014-04, Vol.9 (4), p.e95166</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Ishida et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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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.</description><subject>Adenosine diphosphate</subject><subject>Amoeba</subject><subject>Amoeba - pathogenicity</subject><subject>Amoeba - physiology</subject><subject>Anaplasma phagocytophilum</subject><subject>Ankyrins</subject><subject>ATP</subject><subject>ATP-binding protein</subject><subject>Bacteria</subject><subject>Bacterial genetics</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Chlamydia</subject><subject>Chlamydia - genetics</subject><subject>Chlamydia - pathogenicity</subject><subject>Computer and Information Sciences</subject><subject>Defects</subject><subject>Electron transport</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genome, Bacterial</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Health sciences</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Legionella</subject><subject>Legionella pneumophila - pathogenicity</subject><subject>Legionellosis</subject><subject>Legionnaires' disease</subject><subject>Legionnaires' disease bacterium</subject><subject>Leucine</subject><subject>Lysis</subject><subject>Medical laboratories</subject><subject>Medicine and Health Sciences</subject><subject>Membrane proteins</subject><subject>Metabolic pathways</subject><subject>Molecular Sequence Data</subject><subject>Nucleotide sequence</subject><subject>Outer membrane proteins</subject><subject>Phylogenetics</subject><subject>Protein interaction</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Sexually transmitted diseases</subject><subject>STD</subject><subject>Symbiosis</subject><subject>Tricarboxylic acid 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Fumihiko</au><au>Kuroda, Makoto</au><au>Nakamura, Shinji</au><au>Yamazaki, Tomohiro</au><au>Yoshida, Mitsutaka</au><au>Takahashi, Kaori</au><au>Nagai, Hiroki</au><au>Sugimoto, Chihiro</au><au>Yamaguchi, Hiroyuki</au><au>Horn, Matthias</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Amoebal endosymbiont Neochlamydia genome sequence illuminates the bacterial role in the defense of the host amoebae against Legionella pneumophila</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-04-01</date><risdate>2014</risdate><volume>9</volume><issue>4</issue><spage>e95166</spage><pages>e95166-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24747986</pmid><doi>10.1371/journal.pone.0095166</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2014-04, Vol.9 (4), p.e95166 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1517611333 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adenosine diphosphate Amoeba Amoeba - pathogenicity Amoeba - physiology Anaplasma phagocytophilum Ankyrins ATP ATP-binding protein Bacteria Bacterial genetics Bioinformatics Biology and Life Sciences Chlamydia Chlamydia - genetics Chlamydia - pathogenicity Computer and Information Sciences Defects Electron transport Genes Genetic aspects Genome, Bacterial Genomes Genomics Health sciences Infections Infectious diseases Legionella Legionella pneumophila - pathogenicity Legionellosis Legionnaires' disease Legionnaires' disease bacterium Leucine Lysis Medical laboratories Medicine and Health Sciences Membrane proteins Metabolic pathways Molecular Sequence Data Nucleotide sequence Outer membrane proteins Phylogenetics Protein interaction Proteins Research and Analysis Methods Sexually transmitted diseases STD Symbiosis Tricarboxylic acid cycle University graduates Zoonoses |
| title | Amoebal endosymbiont Neochlamydia genome sequence illuminates the bacterial role in the defense of the host amoebae against Legionella pneumophila |
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