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High Quality Draft Genome Sequence of Mycoplasma Testudineum Strain BH29T, Isolated from the Respiratory Tract of a Desert Tortoise Chava L

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High Quality Draft Genome Sequence of Mycoplasma Testudineum Strain BH29T, Isolated from the Respiratory Tract of a Desert Tortoise Chava L Weitzman et al. Standards in Genomic Sciences (2018) 13:9 https://doi.org/10.1186/s40793-018-0309-z SHORT GENOME REPORT Open Access High quality draft genome sequence of Mycoplasma testudineum strain BH29T, isolated from the respiratory tract of a desert tortoise Chava L. Weitzman1, Richard L. Tillett2, Franziska C. Sandmeier3, C. Richard Tracy1 and David Alvarez-Ponce1* Abstract Mycoplasma testudineum is one of the pathogens that can cause upper respiratory tract disease in desert tortoises, Gopherus agassizii. We sequenced the genome of M. testudineum BH29T (ATCC 700618T = MCCM 03231T), isolated from the upper respiratory tract of a Mojave desert tortoise with upper respiratory tract disease. The sequenced draft genome, organized in 25 scaffolds, has a length of 960,895 bp and a G + C content of 27.54%. A total of 788 protein-coding sequences, six pseudogenes and 35 RNA genes were identified. The potential presence of cytadhesin-encoding genes is investigated. This genome will enable comparative genomic studies to help understand the molecular bases of the pathogenicity of this and other Mycoplasma species. Keywords: Mycoplasma testudineum, Desert tortoise, Gopherus, Upper respiratory tract disease, URTD Introduction the species, we extracted DNA from a culture of the type- Species of the genus Mycoplasma have extremely small strain, BH29T, which was collected from the upper genomes, likely contributing to the need of the species to respiratory tract of a wild Mojave desert tortoise, Gopherus gain resources from host cells, and while Mycoplasma agassizii [3]. This sequencing work is part of a larger project form a variety of relationships with hosts, many are patho- addressing mycoplasmal variation among host species. genic in vertebrates [1]. In North American tortoises, an upper respiratory tract disease is associated with both Organism information Mycoplasma testudineum and its close relative, Myco- Classification and features – plasma agassizii [2 5]. North American tortoise popula- M. testudineum infects the upper respiratory tracts of tor- tions are in decline, with infectious disease as a possible – toises causing upper respiratory tract disease [3, 4]; how- agent in these declines [6 8], though importantly, our ever, recent investigations in wild tortoises suggest it may knowledge of the mechanisms of disease progression and be present in the host without pathogenicity [11]. This mi- its impacts on populations is lacking [9, 10]. To under- crobe has been found in five tortoise species inhabiting stand URTD, we must improve our understanding of the North America—G. agassizii, G. morafkai, G. evgoodei, G. pathogens associated with the disease. By sequencing the berlandieri, and G. polyphemus [3, 11–13]—and its pres- genome of M. testudineum, we may gain insight into pro- ence has yet to be investigated in the sixth tortoise con- teins associated with its pathogenicity and virulence. gener, G. flavomarginatus (located in north-central Until now, DNA sequence data available for this species Mexico). From wild samples, there is some indication that in GenBank was limited to ribosomal RNA genes and the M. testudineum mayhaveafacilitativerelationshipwith associated intergenic spacer region, as well as the RNA M. agassizii in tortoise hosts, but interactions with other polymerase beta subunit gene. To obtain genomic data on community members are unknown [11]. M. testudineum is a sugar-fermenting, coccoid * Correspondence: [email protected] 1Biology Department, University of Nevada, Reno, USA Mycoplasma,whichisverysimilarinphenotypeto Full list of author information is available at the end of the article the closely-related M. agassizii [3](Table1,Fig.1). © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Weitzman et al. Standards in Genomic Sciences (2018) 13:9 Page 2 of 9 Fig. 1 Transmission electron micrograph of thin section of Mycoplasma testudineum strain BH29T.Imagefromref.[3], reproduced with permission from the publisher M. testudineum grows in culture at 22–30°C, with an Genome sequencing information optimal growth at 30°C [3] (Table 1). These tempera- Genome project history tures are frequently experienced in their hosts during The type strain of M. testudineum, strain BH29T,was the seasons when tortoises are found to be most ac- selected for sequencing. This strain was isolated from a tive [14, 15], though tortoise body temperatures can nasal flush of the choana of a Mojave desert tortoise, fluctuate well above or below these temperatures which was filtered through a 0.45 μm filter and then within a day and over the seasons [14–16]. grown in SP4 broth [2, 3]. Sequencing was conducted in To determine the placement of M. testudineum in the October 2016. The Whole Genome Shotgun project was mycoplasmal phylogeny, all 16S rRNA gene sequences deposited at DDBJ/ENA/GenBank under the accession fromthetypestrainsofMycoplasma species were ob- number NNCE00000000. The version described in this tained from the SILVA database [17] and aligned using paper is the first version, NNCE01000000. A summary MUSCLE 3.8.31 [18], and a phylogenetic tree was con- of the project information in compliance with MIGS structed using the maximum likelihood method imple- version 2.0 [25] is shown in Table 2. mented in MEGA7 [19](Fig.2). M. agassizii is a sister group of M. testudineum in the resultant tree, and the Growth conditions and genomic DNA preparation M. testudineum/M. agassizii clade is a sister group of Freeze-dried M. testudineum, strain BH29T,was Mycoplasma pulmonis—the agent of murine respiratory obtained from the ATCC in November 2014 (ATCC mycoplasmosis, which also seems to be present in 700618T) and had been cultured by the ATCC on humans who are in contact with rodents [20]. All Spiroplasma SP4 medium at 30°C in aerobic conditions. three species fall within the hominis group of Myco- Genomic DNA was extracted using the Qiagen DNeasy plasma (see ref. [21] for group definitions). The M. Blood and Tissue Kit protocol for Gram-negative testudineum 16S rRNA gene sequence is 93.1 and 89. bacteria and eluted with ultra-pure water. Extracted 2% identical to those of M. agassizii and M. pulmo- DNA was quantified on a Qiagen QIAxpert system and nis, respectively. Remarkably, these species are not with Picogreen analysis. closely related to Mycoplasma testudinis,isolated from the cloaca of a spur-thighed tortoise (Testudo Genome sequencing and assembly graeca)intheUK[22], which are placed in the pneu- Genome sequencing was conducted using the Illumina moniae group. A previous taxonomic analysis placed Nextera XT DNA Library Preparation Kit (Illumina, Inc., M. testudinis within the pneumoniae group (in agree- San Diego, USA) with the Illumina NextSeq500 platform ment with our results), but placed M. testudineum (150 bp, paired-end) and 2 ng of starting genomic DNA at and M. agassizii in different hominis subgroups: the the Nevada Genomics Center (University of Nevada, Reno). hyorhinis and the fermentans groups, respectively Sequencing was performed in multiplex with multiple sam- [23]. Our result is, however, in agreement with that ples, using dual index sequences from the Illumina Nextera by Volokhov et al. [24], which was also based on 16S XT Index Kit, v2 (index 1, N701; index 2, S502). A total of rRNA data. 455,422 read pairs were obtained. Using Trimmomatic, Weitzman et al. Standards in Genomic Sciences (2018) 13:9 Page 3 of 9 Table 1 Classification and general features of Mycoplasma testudineum strain BH29T MIGS ID Property Term Evidence codea Classification Domain Bacteria TAS [48] Phylum “Tenericutes” TAS [49] Class Mollicutes TAS [50] Order Mycoplasmatales TAS [51, 52] Family Mycoplasmataceae TAS [52] Genus Mycoplasma TAS [53, 54] Species Mycoplasma testudineum TAS [3] Type strain: BH29T Gram stain Negative TAS [3] Cell shape Coccoid to pleomorphic TAS [3] Motility Non-motile TAS [3] Sporulation Nonspore-forming NAS Temperature range 22–30 °C TAS [3] Optimum temperature 30 °C TAS [3] pH range; Optimum Not reported NAS Carbon source Glucose, mannose, lactose, sucrose TAS [3] MIGS-6 Habitat Tortoise respiratory tract TAS [3] MIGS-6.3 Salinity Not reported NAS MIGS-22 Oxygen requirement Aerobic TAS [3] MIGS-15 Biotic relationship Symbiont TAS [3] MIGS-14 Pathogenicity Pathogenic TAS [3, 4] MIGS-4 Geographic location North America TAS [3] MIGS-5 Sample collection 1995 TAS [3, 23] MIGS-4.1 Latitude Not reported, BH29T from Mojave Desert, USA TAS [3] MIGS-4.2 Longitude N/A NAS MIGS-4.4 Altitude N/A NAS aEvidence codes - IDA Inferred from Direct Assay, TAS Traceable Author Statement (i.e., a direct report exists in the literature), NAS Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from the Gene Ontology project [55] version 0.36 [26], reads were trimmed to remove Nextera [28]. For each predicted protein, (i) families were adapter sequences and low quality nucleotides from either identified using the Pfam 31.0 [29] batch search tool end (average Phred score Q ≤ 5, four bp sliding window), (“gathering threshold” option), (ii)COGcategories and sequences trimmed to < 35 bp were removed. After were assigned using eggNOG-mapper [30]basedon trimming, 412,763 read pairs and 36,907 single-reads (the eggNOG 4.5.1 data [31], (iii) signal peptides were pairs of which were removed) remained. De novo genome identified using the SignalP server 4.1 [32], and (iv) assembly was performed using SPAdes 3.10.1 [27], using as transmembrane helices were inferred using the inputs the trimmed paired reads, and the trimmed single TMHMM server v.
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