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Mycoplasma Haemocanis the Canine Hemoplasma and Its Feline

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Mycoplasma Haemocanis the Canine Hemoplasma and Its Feline do Nascimento et al. Veterinary Research 2012, 43:66 http://www.veterinaryresearch.org/content/43/1/66 VETERINARY RESEARCH RESEARCH Open Access Mycoplasma haemocanis – the canine hemoplasma and its feline counterpart in the genomic era Naíla C do Nascimento1*, Andrea P Santos1, Ana MS Guimaraes1, Phillip J SanMiguel2 and Joanne B Messick1* Abstract Mycoplasma haemocanis is a hemotrophic mycoplasma (hemoplasma), blood pathogen that may cause acute disease in immunosuppressed or splenectomized dogs. The genome of the strain Illinois, isolated from blood of a naturally infected dog, has been entirely sequenced and annotated to gain a better understanding of the biology of M. haemocanis. Its single circular chromosome has 919 992 bp and a low G + C content (35%), representing a typical mycoplasmal genome. A gene-by-gene comparison against its feline counterpart, M. haemofelis, reveals a very similar composition and architecture with most of the genes having conserved synteny extending over their entire chromosomes and differing only by a small set of unique protein coding sequences. As in M. haemofelis, M. haemocanis metabolic pathways are reduced and apparently rely heavily on the nutrients afforded by its host environment. The presence of a major percentage of its genome dedicated to paralogous genes (63.7%) suggests that this bacterium might use antigenic variation as a mechanism to evade the host’s immune system as also observed in M. haemofelis genome. Phylogenomic comparisons based on average nucleotide identity (ANI) and tetranucleotide signature suggest that these two pathogens are different species of mycoplasmas, with M. haemocanis infecting dogs and M. haemofelis infecting cats. Introduction immunosuppressed [5,9] or splenectomized dogs [5,10], Hemotrophic mycoplasmas (hemoplasmas) are uncultiv- and has a worldwide distribution with prevalence of able cell-wall less bacteria, formerly classified as Haemo- infection varying from 0.5% to 40% [11-14]. bartonella and Eperythrozoon species, that adhere to the Similarities with the feline hemoplasma M. haemofelis surface of the erythrocytes of their vertebrate hosts. [Haemobartonella felis], together with the fact that hemo- These bacteria form a new clade within the Mycoplasma plasmas are not species-specific as previously thought genus (class Mollicutes) and are phylogenetically related [15,16], led some research groups to hypothesize that to the pneumoniae group of the mycoplasmas [1-5]. these two bacteria could be the same species infecting Mycoplasma haemocanis [Haemobartonella canis]was different hosts [17,18]. Moreover, there are some reports first described in Germany in 1928 in a splenectomized in the old literature stating that M. haemocanis could dog [6]. The name Bartonella canis was proposed and infect cats; however M. haemofelis did not cause infection remained until 1939 when Tyzzer and Weinman created in dogs [19-21]. In 1961, Dr Lumb published the manu- the new genus Haemobartonella [7]. M. haemocanis, script “Canine haemobartonellosis and its feline counter- proposed species name since 2002 [5], is a pleomorphic part”, reporting cross-transmission experiments: it was bacterium with coccoid and ring forms that can be shown that when blood from cats infected with M. haemo- visualized in the host’s peripheral blood smear either canis was injected into susceptible splenectomized dogs, singly or in chains that can resemble a “violin-bow” organisms could be seen on their peripheral blood smears form [8]. It may cause overt, hemolytic anemia in [8]. It was concluded based on this evidence that the feline might act as a reservoir for M. haemocanis. However, blood * Correspondence: [email protected]; [email protected] from dogs previously injected with M. haemofelis inocu- 1Department of Veterinary Pathobiology, Purdue University, 725 Harrison Street, West Lafayette, IN 47907, USA lated into susceptible cats failed to result in circulating Full list of author information is available at the end of the article © 2012 do Nascimento et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. do Nascimento et al. Veterinary Research 2012, 43:66 Page 2 of 9 http://www.veterinaryresearch.org/content/43/1/66 organisms, leading to the conclusion that these two bacteria performed based on genomic data deposited in the were different species [8,22]. Forty years later, the sequences NCBI database (NCBI, Bethesda, MD, USA). of the 16S rRNA genes of these two bacteria were reported The assignment of paralogous gene families was per- to have 99% identity [17] raising the same question again. formed using BLASTclust tool provided by Max-Planck In 2002, the sequences of the RNase P genes of these bac- Institute for Developmental Biology [29], with 70% cov- teriawerereportedhaving94.3 to 95.5% identity [18]. ered length and 30% sequence identity thresholds. Sub- While the results of the RNase P genes did not support the cellular localization and protein sorting signals were hypothesis that M. haemocanis and M. haemofelis were predicted for each unique protein coding sequence identical, this additional data was still considered insuffi- (CDS) of M. haemocanis and M. haemofelis using cient to determine whether these organisms should be clas- PSORTb v.3.0 [30,31]. Metabolic pathways were pre- sified as different species, subspecies, or strains of the same dicted based on the KEGG pathway database [32] and species [18]. the study reported by Yus et al. [33]. Presence of lipo- Recently, three species of hemoplasmas, including proteins was predicted by LipoP version 1.0 software M. haemofelis, had their genomes completely sequenced [34]. In addition, the tandem repeats were identified and annotated [23-27]. The aim of this study was to using the Tandem repeats finder program [35]. Com- sequence the whole genome of M. haemocanis in order to parative analyses of the whole genome of M. haemocanis better understand its biology and to perform a complete and M. haemofelis strain Ohio2 were performed using genomic comparison with its counterpart, M. haemofelis. the same tools mentioned above and all the CDSs from both genomes were evaluated using BLASTp and/or Materials and methods BLASTn in order to obtain a complete detailed compari- Bacterial strain and DNA isolation son. CDSs were assigned using BLASTp and considered M. haemocanis M. haemofelis M. haemocanis organisms were isolated from the blood unique to or when there of a naturally infected dog at peak of bacteremia [17]. were no matching sequences in the aligned sequences ≥ ≥ ≥ Written informed consent was obtained from the client list with 90% coverage and 30% identity or 80% ≥ for publication of this report. Bacterial genomic DNA coverage and 40% identity to the query sequence. was extracted using Quick-gDNA MiniPrep kit accord- Extended similarity group method for automated protein ing to the manufacturer’s instructions (Zymo Research, function prediction (ESG software) [36] was applied for Irvine, CA, USA). both sets of unique CDSs. Species differentiation analyses M. haemocanis strain Illinois sequencing and assembly The average nucleotide identity (ANI; MUMmer algo- Whole genome was sequenced from paired-end libraries rithm) and tetranucleotide signature correlation index (TruSeq DNA sample preparation kit, Illumina, San W between genomes were calculated using JSpecies software Diego, CA, USA) using 20% of an Illumina v3 chemis- as previously described [37]. In addition to the genome of try lane (HiScanSQ). Sequencing resulted in 15.7 million M. haemocanis strain Illinois, the following genome high-quality filtered read pairs with an average read sequences were used in the analyses: M. haemofelis strain length of 2 × 100 nucleotides and a > 3400 X genome Ohio2 (CP002808.1), M. haemofelis strain Langford equivalent coverage. Reads were assembled using (FR773153.2), M. suis strain Illinois (CP002525.1), and M. “ ” ABySS-PE v1.2.7 utilizing 20% of the reads with kmer suis strain KI3806 (FQ790233.1). If two organisms had set to 95 bases [28]. Predicted scaffolds with significant ANIm and tetranucleotide coefficients greater than 94% BLAST matches to canine DNA were excluded and the and 0.99, respectively, they were considered the same remaining mycoplasma scaffolds were then organized species [37]. based on the orientation predicted in the assembly and M. haemofelis on the genome sequence of strain Ohio2. Results A total of 13 gaps were identified and closed using con- Mycoplasma haemocanis strain Illinois genome features ventional PCR followed by Sanger sequencing. The complete singular circular chromosome of M. hae- mocanis strain Illinois has a size of 919 992 base pairs Genome annotation and analyses (bp) and G + C content of 35%; these genomic features First pass annotation was achieved using the NCBI an- are similar to other hemoplasmas species sequenced to notation pipeline. Manual annotation/curation of each date [23,24,26,27] and within the range reported for gene was performed using the annotation tool Manatee, other members of the genus Mycoplasma (Table 1). As provided by the Institute for Genome Sciences (IGS) at described for all sequenced mycoplasmas (24 species to the University of Maryland, School of Medicine. Com- date), M. haemocanis also uses the opal stop codon
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