Phylogenetic and comparative genomics of the family Leptotrichiaceae and introduction of a novel fingerprinting MLVA for Streptobacillus moniliformis

BackgroundThe Leptotrichiaceae are a family of fairly unnoticed bacteria containing both microbiota on mucous membranes as well as significant pathogens such as Streptobacillus moniliformis, the causative organism of streptobacillary rat bite fever. Comprehensive genomic studies in members of this family have so far not been carried out. We aimed to analyze 47 genomes from 20 different member species to illuminate phylogenetic aspects, as well as genomic and discriminatory properties.ResultsOur data provide a novel and reliable basis of support for previously established phylogeny from this group and give a deeper insight into characteristics of genome structure and gene functions. Full genome analyses revealed that most S. moniliformis strains under study form a heterogeneous population without any significant clustering. Analysis of infra-species variability for this highly pathogenic rat bite fever organism led to the detection of three specific variable number tandem analysis loci with high discriminatory power.ConclusionsThis highly useful and economical tool can be directly employed in clinical samples without laborious prior cultivation. Our and prospective case-specific data can now easily be compared by using a newly established MLVA database in order to gain a better insight into the epidemiology of this presumably under-reported zoonosis.

[1]  Jennifer M. Fettweis,et al.  Genomic sequence analysis and characterization of Sneathia amnii sp. nov , 2012, BMC Genomics.

[2]  Root sepsis associated with insect-dwelling Sebaldella termitidis in a lesser dwarf lemur (Cheirogaleus medius) , 2015, Antonie van Leeuwenhoek.

[3]  N. Kyrpides,et al.  Complete genome sequence of Sebaldella termitidis type strain (NCTC 11300T) , 2010, Standards in genomic sciences.

[4]  Nikos Kyrpides,et al.  Genome Sequence and Analysis of the Oral Bacterium Fusobacterium nucleatum Strain ATCC 25586 , 2002, Journal of bacteriology.

[5]  S. Gharbia,et al.  Approaches to the study of the systematics of anaerobic, gram-negative, non-sporeforming rods: current status and perspectives. , 2009, Anaerobe.

[6]  S. Moon,et al.  Application of rpoB and Zinc Protease Gene for Use in Molecular Discrimination of Fusobacterium nucleatum Subspecies , 2009, Journal of Clinical Microbiology.

[7]  D. Relman,et al.  Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea , 2016, Nature Communications.

[8]  R. Boot,et al.  PCR for the detection of Streptobacillus moniliformis , 2002, Laboratory animals.

[9]  T. Haga,et al.  Phylogenetic analysis of Fusobacterium necrophorum, Fusobacterium varium and Fusobacterium nucleatum based on gyrB gene sequences. , 2004, The Journal of veterinary medical science.

[10]  G. T. Clark,et al.  Streptobacillus moniliformis infection in turkeys , 1966, Veterinary Record.

[11]  P. Lawson,et al.  Intrageneric relationships of members of the genus Fusobacterium as determined by reverse transcriptase sequencing of small-subunit rRNA. , 1991, International journal of systematic bacteriology.

[12]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[13]  Hongbin Wang,et al.  Identification of a 43-kDa outer membrane protein of Fusobacterium necrophorum that exhibits similarity with pore-forming proteins of other Fusobacterium species. , 2013, Research in veterinary science.

[14]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[15]  C. Ewers,et al.  Caviibacter abscessus gen. nov., sp. nov., a member of the family Leptotrichiaceae isolated from guinea pigs (Cavia porcellus). , 2016, International journal of systematic and evolutionary microbiology.

[16]  Lynne A. Goodwin,et al.  Complete genome sequence of Streptobacillus moniliformis type strain (9901T) , 2009, Standards in genomic sciences.

[17]  Radhey S. Gupta,et al.  Phylogeny and molecular signatures for the phylum Fusobacteria and its distinct subclades. , 2014, Anaerobe.

[18]  J. Steiner,et al.  Molecular-phylogenetic characterization of microbial communities imbalances in the small intestine of dogs with inflammatory bowel disease. , 2008, FEMS microbiology ecology.

[19]  N. Pochet,et al.  Sequence-based estimation of minisatellite and microsatellite repeat variability. , 2007, Genome research.

[20]  S. Achenbach,et al.  Fulminant endocarditis caused by Streptobacillus moniliformis in a young man. , 2007, The Journal of thoracic and cardiovascular surgery.

[21]  C. Ewers,et al.  Oceanivirga salmonicida gen. nov., sp. nov., a member of the Leptotrichiaceae isolated from Atlantic salmon (Salmo salar). , 2016, International journal of systematic and evolutionary microbiology.

[22]  E. Allen-Vercoe,et al.  Phenotypic and genotypic analyses of clinical Fusobacterium nucleatum and Fusobacterium periodonticum isolates from the human gut. , 2008, Anaerobe.

[23]  W. Gaastra,et al.  Rat bite fever. , 2009, Veterinary microbiology.

[24]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[25]  W. Gaastra,et al.  Dogs as vectors of Streptobacillus moniliformis infection? , 2008, Veterinary microbiology.

[26]  Narmada Thanki,et al.  CDD: NCBI's conserved domain database , 2014, Nucleic Acids Res..

[27]  Samson S. Y. Wong,et al.  Leptotrichia hongkongensis sp. nov., a novel Leptotrichia species with the oral cavity as its natural reservoir , 2010, Journal of Zhejiang University SCIENCE B.

[28]  C. Ewers,et al.  Phenotypic and Genotypic Characteristics of Members of the Genus Streptobacillus , 2015, PloS one.

[29]  M. Collins,et al.  Characterization of some strains from human clinical sources which resemble "Leptotrichia sanguinegens": description of Sneathia sanguinegens sp. nov., gen. nov. , 2001, Systematic and applied microbiology.

[30]  C. Ewers,et al.  Approved and novel strategies in diagnostics of rat bite fever and other Streptobacillus infections in humans and animals , 2016, Virulence.

[31]  R. Jáuregui,et al.  The microbial community structure of the cotton rat nose. , 2015, Environmental microbiology reports.

[32]  C. Yeoman,et al.  Characterization of the Vaginal Microbiota of Ewes and Cows Reveals a Unique Microbiota with Low Levels of Lactobacilli and Near-Neutral pH , 2014, Front. Vet. Sci..

[33]  C. Ewers,et al.  Streptobacillus ratti sp. nov., isolated from a black rat (Rattus rattus). , 2016, International journal of systematic and evolutionary microbiology.

[34]  F. Dewhirst,et al.  The Canine Oral Microbiome , 2012, PloS one.

[35]  J. Lloyd,et al.  Streptobacillus moniliformis septicaemia in spinifex hopping mice (Notomys alexis) , 1981, Australian veterinary journal.

[36]  S. Dowd,et al.  Amplicon pyrosequencing of wild duck eubacterial microbiome from a fecal sample reveals numerous species linked to human and animal diseases , 2013 .

[37]  Rick L. Stevens,et al.  The RAST Server: Rapid Annotations using Subsystems Technology , 2008, BMC Genomics.

[38]  C. Ewers,et al.  Streptobacillus notomytis sp. nov., isolated from a spinifex hopping mouse (Notomys alexis Thomas, 1922), and emended description of Streptobacillus Levaditi et al. 1925, Eisenberg et al. 2015 emend. , 2015, International journal of systematic and evolutionary microbiology.

[39]  Terry J. Smith,et al.  Relationship of a Novel Bacterial Fish Pathogen to Streptobacillus moniliformis and the Fusobacteria , 1995 .

[40]  N. L. Baumgart,et al.  A model for curriculum evaluation , 1972 .

[41]  J. Jalava,et al.  Phylogenetic analysis of Fusobacterium alocis and Fusobacterium sulci based on 16S rRNA gene sequences: proposal of Filifactor alocis (Cato, Moore and Moore) comb. nov. and Eubacterium sulci (Cato, Moore and Moore) comb. nov. , 1999, International journal of systematic bacteriology.

[42]  P. Woo,et al.  Streptobacillus hongkongensis sp. nov., isolated from patients with quinsy and septic arthritis, and emended descriptions of the genus Streptobacillus and Streptobacillus moniliformis. , 2014, International journal of systematic and evolutionary microbiology.

[43]  T. Eisenberg,et al.  Streptobacillus sp. isolated from a cat with pneumonia , 2014 .

[44]  Julia Oh,et al.  Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis , 2012, Genome research.

[45]  J. Kaspareit-Rittinghausen,et al.  Streptobacillus moniliformis epizootic in barrier-maintained C57BL/6J mice and susceptibility to infection of different strains of mice. , 1990, Laboratory animal science.

[46]  Complete genome sequence of Leptotrichia buccalis type strain (C-1013-bT) , 2009, Standards in genomic sciences.

[47]  J. Corander,et al.  Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution , 2014, Nature Genetics.

[48]  P. Kämpfer,et al.  Streptobacillus felis sp. nov., isolated from a cat with pneumonia, and emended descriptions of the genus Streptobacillus and of Streptobacillus moniliformis. , 2015, International journal of systematic and evolutionary microbiology.

[49]  T. Murphy,et al.  A previously unknown disease of farmed Atlantic salmon: pathology and establishment of bacterial aetiology , 1994 .

[50]  F. Dewhirst,et al.  Genetic diversity of Leptotrichia and description of Leptotrichia goodfellowii sp. nov., Leptotrichia hofstadii sp. nov., Leptotrichia shahii sp. nov. and Leptotrichia wadei sp. nov. , 2004, International journal of systematic and evolutionary microbiology.

[51]  E. Goldstein,et al.  16S-23S rDNA internal transcribed spacer sequences for analysis of the phylogenetic relationships among species of the genus Fusobacterium. , 2002, International journal of systematic and evolutionary microbiology.

[52]  C. Jonas,et al.  Streptobacillus moniliformis isolated from otitis media of conventionally kept laboratory rats. , 1992, Journal of experimental animal science.

[53]  A. Yamada,et al.  Detection of Streptobacillus spp. in feral rats by specific polymerase chain reaction , 2008, Microbiology and immunology.

[54]  K. Wilson,et al.  Leptotrichia sanguinegens sp. nov., a new agent of postpartum and neonatal bacteremia. , 1995, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[55]  K. Newton,et al.  Enterolignan-Producing Phenotypes Are Associated with Increased Gut Microbial Diversity and Altered Composition in Premenopausal Women in the United States , 2014, Cancer Epidemiology, Biomarkers & Prevention.

[56]  B. La Scola,et al.  Shell vial cell culture as a tool for Streptobacillus moniliformis "resuscitation". , 2011, The American journal of tropical medicine and hygiene.

[57]  Lukas Wagner,et al.  A Greedy Algorithm for Aligning DNA Sequences , 2000, J. Comput. Biol..