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Life on Arginine for Mycoplasma Hominis: Clues from Its Minimal Genome and Comparison with Other Human Urogenital Mycoplasmas

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Life on Arginine for Mycoplasma Hominis: Clues from Its Minimal Genome and Comparison with Other Human Urogenital Mycoplasmas Life on arginine for Mycoplasma hominis: clues from its minimal genome and comparison with other human urogenital mycoplasmas. Sabine Pereyre, Pascal Sirand-Pugnet, Laure Beven, Alain Charron, Hélène Renaudin, Aurélien Barré, Philippe Avenaud, Daniel Jacob, Arnaud Couloux, Valérie Barbe, et al. To cite this version: Sabine Pereyre, Pascal Sirand-Pugnet, Laure Beven, Alain Charron, Hélène Renaudin, et al.. Life on arginine for Mycoplasma hominis: clues from its minimal genome and comparison with other human urogenital mycoplasmas.. PLoS Genetics, Public Library of Science, 2009, 5 (10), pp.e1000677. 10.1371/journal.pgen.1000677. hal-00645937 HAL Id: hal-00645937 https://hal.archives-ouvertes.fr/hal-00645937 Submitted on 31 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Life on Arginine for Mycoplasma hominis: Clues from Its Minimal Genome and Comparison with Other Human Urogenital Mycoplasmas Sabine Pereyre1, Pascal Sirand-Pugnet2,3, Laure Beven2,3, Alain Charron1,He´le`ne Renaudin1, Aure´lien Barre´ 4, Philippe Avenaud1, Daniel Jacob4, Arnaud Couloux6, Vale´rie Barbe6, Antoine de Daruvar4,5, Alain Blanchard2,3,Ce´cile Be´be´ar1* 1 Universite´ de Bordeaux, Laboratoire de Bacte´riologie EA 3671, Bordeaux, France, 2 INRA, UMR 1090, Villenave d’Ornon, France, 3 Universite´ de Bordeaux, UMR 1090, Villenave d’Ornon, France, 4 Universite´ de Bordeaux, Centre de Bioinformatique de Bordeaux, Bordeaux, France, 5 CNRS UMR 5800, Laboratoire Bordelais de Recherche en Informatique, Talence, France, 6 Ge´noscope, Centre National de Se´quenc¸age, Evry, France Abstract Mycoplasma hominis is an opportunistic human mycoplasma. Two other pathogenic human species, M. genitalium and Ureaplasma parvum, reside within the same natural niche as M. hominis: the urogenital tract. These three species have overlapping, but distinct, pathogenic roles. They have minimal genomes and, thus, reduced metabolic capabilities characterized by distinct energy-generating pathways. Analysis of the M. hominis PG21 genome sequence revealed that it is the second smallest genome among self-replicating free living organisms (665,445 bp, 537 coding sequences (CDSs)). Five clusters of genes were predicted to have undergone horizontal gene transfer (HGT) between M. hominis and the phylogenetically distant U. parvum species. We reconstructed M. hominis metabolic pathways from the predicted genes, with particular emphasis on energy-generating pathways. The Embden–Meyerhoff–Parnas pathway was incomplete, with a single enzyme absent. We identified the three proteins constituting the arginine dihydrolase pathway. This pathway was found essential to promote growth in vivo. The predicted presence of dimethylarginine dimethylaminohydrolase suggested that arginine catabolism is more complex than initially described. This enzyme may have been acquired by HGT from non- mollicute bacteria. Comparison of the three minimal mollicute genomes showed that 247 CDSs were common to all three genomes, whereas 220 CDSs were specific to M. hominis, 172 CDSs were specific to M. genitalium, and 280 CDSs were specific to U. parvum. Within these species-specific genes, two major sets of genes could be identified: one including genes involved in various energy-generating pathways, depending on the energy source used (glucose, urea, or arginine) and another involved in cytadherence and virulence. Therefore, a minimal mycoplasma cell, not including cytadherence and virulence-related genes, could be envisaged containing a core genome (247 genes), plus a set of genes required for providing energy. For M. hominis, this set would include 247+9 genes, resulting in a theoretical minimal genome of 256 genes. Citation: Pereyre S, Sirand-Pugnet P, Beven L, Charron A, Renaudin H, et al. (2009) Life on Arginine for Mycoplasma hominis: Clues from Its Minimal Genome and Comparison with Other Human Urogenital Mycoplasmas. PLoS Genet 5(10): e1000677. doi:10.1371/journal.pgen.1000677 Editor: Josep Casadesu´s, Universidad de Sevilla, Spain Received May 19, 2009; Accepted September 7, 2009; Published October 9, 2009 Copyright: ß 2009 Pereyre et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported by internal funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction and Ureaplasma spp., but not M. hominis, are involved in male urethritis. M. genitalium is also the only mycoplasmal species Mycoplasma hominis is an opportunistic human mycoplasma involved in cervicitis, whereas Ureaplasma spp. are significantly species which resides, as a commensal, in the lower urogenital associated with prematurity, low birth weight and chronic lung tract. However, it can also cause pelvic inflammatory disease and disease in infants [1]. These three urogenital species belong to two postpartum or postabortion fevers, and has been associated with different phylogenetic groups within the class Mollicutes: M. bacterial vaginosis [1]. In newborns, it can cause pneumonia, genitalium and Ureaplasma spp. belong to the Pneumoniae group meningitis or abscesses. It has also been implicated in extragenital and M. hominis belongs to the Hominis group. They possess the infections, especially in immunocompromised patients. smallest genomes among self-replicating free living organisms. The Two other mollicute species, M. genitalium and Ureaplasma M. genitalium genome is the smallest of these, comprising 580 Kbp, urealyticum, the latter having been recently separated into two with a capacity to encode only 482 genes [3]. The minimal nature species U. parvum and U. urealyticum [2], have established of the M. genitalium genome triggered particular interest in this pathogenic roles in humans and reside within the same natural organism and several studies have addressed the concept of a niche, the urogenital tract, as M. hominis. However, these species minimal cell [4–6]. More recent studies have attempted to have overlapping but distinct pathogenic roles [1]. M. genitalium reconstruct its genome by chemical synthesis [7,8], with a view PLoS Genetics | www.plosgenetics.org 1 October 2009 | Volume 5 | Issue 10 | e1000677 Mycoplasma Minimal Genomes Author Summary Table 1. Comparison of general features of the M. hominis genome with those of M. genitalium G37 (ATCC 33530) and U. Mycoplasma hominis, M. genitalium, and Ureaplasma parvum serovar 3 (ATCC 700970). parvum are human pathogenic bacteria that colonize the urogenital tract. They have minimal genomes, and thus have a minimal metabolic capacity. However, they have M. hominis M. genitalium U. parvum distinct energy-generating pathways and distinct patho- Featuresa PG21 G37 serovar 3 genic roles. We compared the genomes of these three human pathogen minimal species, providing further Genome size (bp) 665,445 580,074 751,719 insight into the composition of hypothetical minimal gene GC content of genome (%) 27.1 31.7 25.5 sets needed for life. To this end, we sequenced the whole Gene density (%) 89.8 91.2 91.3 M. hominis genome and reconstructed its energy-gener- ating pathways from gene predictions. Its unusual major Total number of CDS 537 482 614 energy-producing pathway through arginine hydrolysis Hypothetical proteins 106 2 182 was confirmed in both genome analyses and in vivo assays. Conserved hypothetical proteins 86 164 107 Our findings suggest that M. hominis and U. parvum CDSs with predicted fonction 345 316 325 underwent genetic exchange, probably while sharing a b c c common host. We proposed a set of genes likely to Pseudogenes 14 5 0 represent a minimal genome. For M. hominis, this minimal Average protein length (aa) 369 363 371 genome, not including cytadherence and virulence-related Proteins with predicted 2 02 genes, can be defined comprising the 247 genes shared by MW.300 kDa the three minimal genital mollicutes, combined with a set Predicted lipoproteins 43 18d 37d of nine genes needed for energy production for cell rRNA sets 2e 12 metabolism. This study provides insight for the synthesis of artificial genomes. tRNA 33 36 30 Start codon usage (%) AUG 95.1 88.5 92.5 to engineering a new living organism, referred to as Mycoplasma UUG 3.0 4.1 3.0 laboratorium [9]. The genome of M. hominis is slightly larger than GUG 1.7 7.4 4.5 that of M. genitalium, with pulsed-field gel electrophoresis revealing Other 0.2 00 a chromosome size of 696 Kbp [10]. The sequenced genome of U. parvum (previously called U. urealyticum serovar 3) is the largest of Stop codon usage (%) the three species, encompassing 751 Kbp [11]. These three species UAA 83 72 85 can therefore be considered as minimal bacterial cell prototypes UAG 16 27 14 with reduced metabolic abilities. Interestingly, in
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