title: Genetic exchange of fimbrial alleles exemplifies the adaptive virulence strategy of Porphyromonas gingivalis.
abstract: Porphyromonas gingivalis is a gram-negative anaerobic bacterium, a member of the human oral microbiome, and a proposed "keystone" pathogen in the development of chronic periodontitis, an inflammatory disease of the gingiva. P. gingivalis is a genetically diverse species, and is able to exchange chromosomal DNA between strains by natural competence and conjugation. In this study, we investigate the role of horizontal DNA transfer as an adaptive process to modify behavior, using the major fimbriae as our model system, due to their critical role in mediating interactions with the host environment. We show that P. gingivalis is able to exchange fimbrial allele types I and IV into four distinct strain backgrounds via natural competence. In all recombinants, we detected a complete exchange of the entire fimA allele, and the rate of exchange varies between the different strain backgrounds. In addition, gene exchange within other regions of the fimbrial genetic locus was identified. To measure the biological implications of these allele swaps we compared three genotypes of fimA in an isogenic background, strain ATCC 33277. We demonstrate that exchange of fimbrial allele type results in profound phenotypic changes, including the quantity of fimbriae elaborated, membrane blebbing, auto-aggregation and other virulence-associated phenotypes. Replacement of the type I allele with either the type III or IV allele resulted in increased invasion of gingival fibroblast cells relative to the isogenic parent strain. While genetic variability is known to impact host-microbiome interactions, this is the first study to quantitatively assess the adaptive effect of exchanging genes within the pan genome cloud. This is significant as it presents a potential mechanism by which opportunistic pathogens may acquire the traits necessary to modify host-microbial interactions.
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Jennifer E
authors.initials: JE
authors.lastname: Kerr
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Jared R
authors.initials: JR
authors.lastname: Abramian
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Doan-Hieu V
authors.initials: DH
authors.lastname: Dao
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Todd W
authors.initials: TW
authors.lastname: Rigney
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Jamie
authors.initials: J
authors.lastname: Fritz
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Tan
authors.initials: T
authors.lastname: Pham
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Isabel
authors.initials: I
authors.lastname: Gay
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Kavitha
authors.initials: K
authors.lastname: Parthasarathy
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Bing-yan
authors.initials: BY
authors.lastname: Wang
authors.affiliation: Department of Diagnostic and Biomedical Sciences, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Wenjian
authors.initials: W
authors.lastname: Zhang
authors.affiliation: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas Health Science Center at Houston, Houston, Texas, United States of America.
authors.forename: Gena D
authors.initials: GD
authors.lastname: Tribble
mesh_terms: D000483:Alleles; D036781:Fimbriae Proteins / Q000235:genetics / Q000378:metabolism; D010861:Fimbriae, Bacterial / Q000235:genetics*; D022761:Gene Transfer, Horizontal; D014644:Genetic Variation; D005838:Genotype; D006801:Humans; D010518:Periodontitis / Q000235:genetics* / Q000382:microbiology / Q000473:pathology; D010641:Phenotype; D016966:Porphyromonas gingivalis / Q000235:genetics* / Q000472:pathogenicity; D014774:Virulence / Q000235:genetics
chemical_list: D036781:Fimbriae Proteins