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Article: Arginine deiminase pathway is far more important than urease for acid resistance and intracellular survival in Laribacter hongkongensis: a possible result of arc gene cassette duplication

TitleArginine deiminase pathway is far more important than urease for acid resistance and intracellular survival in Laribacter hongkongensis: a possible result of arc gene cassette duplication
Authors
Issue Date2014
PublisherBioMed Central Ltd. The Journal's web site is located at http://www.biomedcentral.com/bmcmicrobiol/
Citation
BMC Microbiology, 2014, v. 14, article no. 42 How to Cite?
AbstractBACKGROUND: Laribacter hongkongensis is a Gram-negative, urease-positive bacillus associated with invasive bacteremic infections in liver cirrhosis patients and fish-borne community-acquired gastroenteritis and traveler's diarrhea. Its mechanisms of adaptation to various environmental niches and host defense evasion are largely unknown. During the process of analyzing the L. hongkongensis genome, a complete urease cassette and two adjacent arc gene cassettes were found. We hypothesize that the urease cassette and/or the arc gene cassettes are important for L. hongkongensis to survive in acidic environment and macrophages. In this study, we tested this hypothesis by constructing single, double and triple non-polar deletion mutants of the urease and two arc gene cassettes of L. hongkongensis using the conjugation-mediated gene deletion system and examining their effects in acidic environment in vitro, in macrophages and in a mouse model. RESULTS: HLHK9ureA, HLHK9ureC, HLHK9ureD and HLHK9ureE all exhibited no urease activity. HLHK9arcA1 and HLHK9arcA2 both exhibited arginine deiminase (ADI) activities, but HLHK9arcA1/arcA2 double deletion mutant exhibited no ADI activity. At pH 2 and 3, survival of HLHK9arcA1/arcA2 and HLHK9ureA/arcA1/arcA2 were markedly decreased (p < 0.001) but that of HLHK9ureA was slightly decreased (p < 0.05), compared to wild type L. hongkongensis HLHK9. Survival of HLHK9ureA/arcA1/arcA2 and HLHK9arcA1/arcA2 in macrophages were also markedly decreased (p < 0.001 and p < 0.01 respectively) but that of HLHK9ureA was slightly decreased (p < 0.05), compared to HLHK9, although expression of arcA1, arcA2 and ureA genes were all upregulated. Using a mouse model, HLHK9ureA exhibited similar survival compared to HLHK9 after passing through the murine stomach, but survival of HLHK9arcA1/arcA2 and HLHK9ureA/arcA1/arcA2 were markedly reduced (p < 0.01). CONCLUSIONS: In contrast to other important gastrointestinal tract pathogens, ADI pathway is far more important than urease for acid resistance and intracellular survival in L. hongkongensis. The gene duplication of the arc gene cassettes could be a result of their functional importance in L. hongkongensis.
Persistent Identifierhttp://hdl.handle.net/10722/200443
ISSN
2015 Impact Factor: 2.581
2015 SCImago Journal Rankings: 1.391
PubMed Central ID
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorXiong, Len_US
dc.contributor.authorTeng, JLLen_US
dc.contributor.authorWatt, RMen_US
dc.contributor.authorKan, BIAOen_US
dc.contributor.authorLau, SKPen_US
dc.contributor.authorWoo, PCYen_US
dc.date.accessioned2014-08-21T06:45:21Z-
dc.date.available2014-08-21T06:45:21Z-
dc.date.issued2014en_US
dc.identifier.citationBMC Microbiology, 2014, v. 14, article no. 42en_US
dc.identifier.issn1471-2180-
dc.identifier.urihttp://hdl.handle.net/10722/200443-
dc.description.abstractBACKGROUND: Laribacter hongkongensis is a Gram-negative, urease-positive bacillus associated with invasive bacteremic infections in liver cirrhosis patients and fish-borne community-acquired gastroenteritis and traveler's diarrhea. Its mechanisms of adaptation to various environmental niches and host defense evasion are largely unknown. During the process of analyzing the L. hongkongensis genome, a complete urease cassette and two adjacent arc gene cassettes were found. We hypothesize that the urease cassette and/or the arc gene cassettes are important for L. hongkongensis to survive in acidic environment and macrophages. In this study, we tested this hypothesis by constructing single, double and triple non-polar deletion mutants of the urease and two arc gene cassettes of L. hongkongensis using the conjugation-mediated gene deletion system and examining their effects in acidic environment in vitro, in macrophages and in a mouse model. RESULTS: HLHK9ureA, HLHK9ureC, HLHK9ureD and HLHK9ureE all exhibited no urease activity. HLHK9arcA1 and HLHK9arcA2 both exhibited arginine deiminase (ADI) activities, but HLHK9arcA1/arcA2 double deletion mutant exhibited no ADI activity. At pH 2 and 3, survival of HLHK9arcA1/arcA2 and HLHK9ureA/arcA1/arcA2 were markedly decreased (p < 0.001) but that of HLHK9ureA was slightly decreased (p < 0.05), compared to wild type L. hongkongensis HLHK9. Survival of HLHK9ureA/arcA1/arcA2 and HLHK9arcA1/arcA2 in macrophages were also markedly decreased (p < 0.001 and p < 0.01 respectively) but that of HLHK9ureA was slightly decreased (p < 0.05), compared to HLHK9, although expression of arcA1, arcA2 and ureA genes were all upregulated. Using a mouse model, HLHK9ureA exhibited similar survival compared to HLHK9 after passing through the murine stomach, but survival of HLHK9arcA1/arcA2 and HLHK9ureA/arcA1/arcA2 were markedly reduced (p < 0.01). CONCLUSIONS: In contrast to other important gastrointestinal tract pathogens, ADI pathway is far more important than urease for acid resistance and intracellular survival in L. hongkongensis. The gene duplication of the arc gene cassettes could be a result of their functional importance in L. hongkongensis.-
dc.languageengen_US
dc.publisherBioMed Central Ltd. The Journal's web site is located at http://www.biomedcentral.com/bmcmicrobiol/-
dc.relation.ispartofBMC Microbiologyen_US
dc.rightsBMC Microbiology. Copyright © BioMed Central Ltd.-
dc.rightsCreative Commons: Attribution 3.0 Hong Kong License-
dc.subject.meshAcids - toxicity-
dc.subject.meshBetaproteobacteria - drug effects - metabolism-
dc.subject.meshGene Duplication-
dc.subject.meshHydrolases - metabolism-
dc.subject.meshMicrobial Viability - drug effects-
dc.titleArginine deiminase pathway is far more important than urease for acid resistance and intracellular survival in Laribacter hongkongensis: a possible result of arc gene cassette duplicationen_US
dc.typeArticleen_US
dc.identifier.emailXiong, L: lfxiong@hku.hken_US
dc.identifier.emailTeng, JLL: llteng@hku.hken_US
dc.identifier.emailWatt, RM: rmwatt@hku.hken_US
dc.identifier.emailLau, SKP: skplau@hkucc.hku.hken_US
dc.identifier.emailWoo, PCY: pcywoo@hkucc.hku.hken_US
dc.identifier.authorityTeng, JLL=rp00277en_US
dc.identifier.authorityWatt, RM=rp00043en_US
dc.identifier.authorityLau, SKP=rp00486en_US
dc.identifier.authorityWoo, PCY=rp00430en_US
dc.description.naturepublished_or_final_version-
dc.identifier.doi10.1186/1471-2180-14-42en_US
dc.identifier.pmid24533585-
dc.identifier.pmcidPMC3936950-
dc.identifier.hkuros234329en_US
dc.identifier.volume14en_US
dc.identifier.isiWOS:000335266000004-
dc.publisher.placeUnited Kingdom-

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