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International Journal of Systematic and Evolutionary Microbiology International Journal of Systematic and Evolutionary Microbiology An evaluation of Thiomicrospira, Hydrogenovibrio and Thioalkalimicrobium: reclassification of 4 species of Thiomicrospira to each Thiomicrorhabdus gen. nov. and Hydrogenovibrio, and reclassification of all 4 species of Thioalkalimicrobium to Thiomicrospira. --Manuscript Draft-- Manuscript Number: IJSEM-D-16-01110R1 Full Title: An evaluation of Thiomicrospira, Hydrogenovibrio and Thioalkalimicrobium: reclassification of 4 species of Thiomicrospira to each Thiomicrorhabdus gen. nov. and Hydrogenovibrio, and reclassification of all 4 species of Thioalkalimicrobium to Thiomicrospira. Article Type: Note Section/Category: New taxa - Proteobacteria Keywords: chemolithoautotroph; Thiomicrospira; Thiomicrorhabdus; Hydrogenovibrio; Thioalkalimicrobium; thiosulfate Corresponding Author: Rich Boden, Ph.D B.Sc (Lond.) PGCert University of Plymouth Plymouth, Devon UNITED KINGDOM First Author: Rich Boden, Ph.D B.Sc (Lond.) PGCert Order of Authors: Rich Boden, Ph.D B.Sc (Lond.) PGCert Kathleen M Scott John T Williams Sydney Russell Kirsten Antonen Alex W Rae Lee P Hutt, Ph.D Manuscript Region of Origin: UNITED KINGDOM Abstract: Thiomicrospira spp. are small sulfur-oxidising chemolithoautotrophic members of the Gammaproteobacteria. Whilst the type species Tms. pelophila and closely related Tms. thyasirae exhibit canonical spiral morphology under sub-optimal growth conditions, most species are vibrios or rods. The 16S rRNA gene diversity is vast, with identities as low as 91.6 % to Tms. pelophila versus Tms. frisia, for example. Thiomicrospira was examined with closely related genera Hydrogenovibrio and Thioalkalimicrobium and, to rationalise organisms on the basis of the 16S rRNA gene phylogeny, physiology and morphology, we reclassify Tms. kuenenii, Tms. crunogena, Tms. thermophila and Tms. halophila to Hydrogenovibrio kuenenii comb. nov., H. crunogenus corrig. comb. nov., H. thermophilus corrig. comb. nov., and H. halophilus corrig. comb. nov. We reclassify Tms. frisia, Tms. arctica, Tms. psychrophila and Tms. chilensis to Thiomicrorhabdus gen. nov., as Tmr. frisia comb. nov., Tmr. arctica comb. nov., Tmr. psychrophila comb. nov. and Tmr. chilensis comb. nov. - the type species of Thiomicrorhabdus is Tmr. frisia. We demonstrate Thioalkalimicrobium spp. fall in the genus Thiomicrospira sensu stricto, thus reclassifying them to Tms. aerophila corrig. comb. nov., Tms. microaerophila corrig. comb. nov., Tms. cyclica corrig. comb. nov.and Tms. sibirica corrig. comb. nov. We provide emended descriptions of the genera Thiomicrospira and Hydrogenovibrio and of Tms. thyasirae. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation Manuscript Including References (Word document) Click here to download Manuscript Including References (Word document) R1 BLACK FINAL Thiomicrospira sensu 1 An evaluation of Thiomicrospira, Hydrogenovibrio and 2 Thioalkalimicrobium: reclassification of 4 species of 3 Thiomicrospira to each Thiomicrorhabdus gen. nov. and 4 Hydrogenovibrio, and reclassification of all 4 species of 5 Thioalkalimicrobium to Thiomicrospira. 6 Rich Boden1,2*, Kathleen M. Scott3, John Williams3, Sydney Russel3, Kirsten 7 Antonen3, Alex W. Rae1 and Lee P. Hutt1,2 8 1. School of Biological & Marine Sciences, University of Plymouth, Drake Circus, Plymouth, 9 UK. 10 2. Sustainable Earth Institute, University of Plymouth, Drake Circus, Plymouth, UK. 11 3. Department of Integrative Biology, University of South Florida, East Fowler Avenue, 12 Tampa, Florida, USA. 13 * Corresponding author [email protected] 14 KEYWORDS: Chemolithoautotroph, Thiomicrospira, Thiomicrorhabdus, Hydrogenovibrio, 15 Thioalkalimicrobium, thiosulfate 16 RUNNING TITLE: Reclassification of Thiomicrospira spp. and Thioalkalimicrobium spp. 17 ABBREVIATIONS: We have used 3-letter abbreviations for genera with similar names, 18 namely Thiomicrospira (Tms.), Thiomicrorhabdus (Tmr.) and Thioalkalimicrobium (Tam.) 19 and retain a single letter for Thiobacillus (T.). Similarly, we refer to Halothiobacillus with 3- 20 letters (Htb.) as we used the single letter for Hydrogenovibrio (H.). 21 1 22 Abstract 23 Thiomicrospira spp. are small sulfur-oxidising chemolithoautotrophic members of the 24 Gammaproteobacteria. Whilst the type species Tms. pelophila and closely related Tms. 25 thyasirae exhibit canonical spiral morphology under sub-optimal growth conditions, most 26 species are vibrios or rods. The 16S rRNA gene diversity is vast, with identities as low as 27 91.6 % to Tms. pelophila versus Tms. frisia, for example. Thiomicrospira was examined with 28 closely related genera Hydrogenovibrio and Thioalkalimicrobium and, to rationalise 29 organisms on the basis of the 16S rRNA gene phylogeny, physiology and morphology, we 30 reclassify Tms. kuenenii, Tms. crunogena, Tms. thermophila and Tms. halophila to 31 Hydrogenovibrio kuenenii comb. nov., H. crunogenus corrig. comb. nov., H. thermophilus 32 corrig. comb. nov., and H. halophilus corrig. comb. nov. We reclassify Tms. frisia, Tms. 33 arctica, Tms. psychrophila and Tms. chilensis to Thiomicrorhabdus gen. nov., as Tmr. frisia 34 comb. nov., Tmr. arctica comb. nov., Tmr. psychrophila comb. nov. and Tmr. chilensis comb. 35 nov. – the type species of Thiomicrorhabdus is Tmr. frisia. We demonstrate 36 Thioalkalimicrobium spp. fall in the genus Thiomicrospira sensu stricto, thus reclassifying 37 them to Tms. aerophila corrig. comb. nov., Tms. microaerophila corrig. comb. nov., Tms. 38 cyclica corrig. comb. nov.and Tms. sibirica corrig. comb. nov. We provide emended 39 descriptions of the genera Thiomicrospira and Hydrogenovibrio and of Tms. thyasirae. 2 40 The genus Thiomicrospira (Kuenen & Veldkamp, 1972; Approved Lists, 1980) falls within 41 the family Piscirickettsiaceae in the order Thiorichales of the class Gammaproteobacteria. It 42 was circumscribed originally by Kuenen & Veldkamp (1972) on the basis of one isolate (Tms. 43 pelophila – a sulfur-oxidising obligate chemolithoautotroph), which had unique properties 44 versus Thiobacillus spp., viz. thinner, spiral or comma-shaped cells and a very high tolerance 45 of sulfide versus T. thioparus, and could be isolated by passing samples through a 0.22 μm 46 filter (Tms. pelophila 0.2 – 0.3 μm diameter). There are currently 10 species with validly 47 published names (Figure 1a), showing considerable metabolic and morphological diversity. 48 Closely affiliated to this genus on the basis of 16S rRNA gene sequences are the 49 monospecific genus Hydrogenovibrio (Nishihara et al., 1991), comprising one hydrogen- 50 oxidising chemolithoautotroph (which also uses sulfur species) and the genus 51 Thioalkalimicrobium (Sorokin et al., 2001, also referred to for a time as 52 “Thialkalimicrobium”), comprising several obligately alkaliphilic sulfur-oxidising 53 chemolithoautotrophs. On the basis of the 16S rRNA (rrs) gene (as shown in Figure 1a), the 54 genus Thiomicrospira currently falls into 3 clades – for the purposes of this study, we refer to 55 them as “Clade A” (Tms. pelophila [type species], Tms. thyasirae, Tam. aerophilum [type 56 species], Tam. microaerophilum, Tam. cyclicum and Tam. sibiricum), “Clade B” (Tms. frisia, 57 Tms. chilensis, Tms. arctica, Tms. psychrophila) and “Clade C” (Tms. thermophila, Tms. 58 crunogena, Tms. kuenenii and H. marinus [type species]). As can be seen from Figure 1a, 59 there is considerable phylogenetic distance between Clade A and Clade B or Clade C (e.g. 60 16S rRNA gene identity Tms. pelophila to Tms. arctica, 92.9%, and to Tms. crunogena, 61 92.1%), and members of the genus Thioalkalimicrobium are more closely related to the type 62 species of Thiomicrospira than members of Clade B or Clade C are (gene identities of Tms. 63 pelophila to Thioalkalimicrobium spp. range from 95.9 to 97.3 %). As such, here we evaluate 64 the taxonomy and systematics of Thiomicrospira, Hydrogenovibrio and Thioalkalimicrobium 3 65 using a polyphasic approach to rationalise species and to circumscribe a novel genus, 66 Thiomicrorhabdus gen. nov. We also expand Hydrogenovibrio to circumscribe other species, 67 currently regarded as Thiomicrospira spp. Furthermore, we also confirm that 68 Thioalkalimicrobium is not distinct from Thiomicrospira and thus reclassify all 4 species into 69 Thiomicrospira. Accordingly, we provide emended descriptions of Thiomicrospira and 70 Hydrogenovibrio and of Tms. thyasirae. 71 Two principle phylogenetic analyses were performed – Figure 1a shows a maximum 72 likelihood tree (Tamura-Nei model) of 16S rRNA genes from species of the 3 genera 73 considered here, restricted to type strains of species with validly published names, using that 74 from Galenea microaerophila P2DT, also from the Piscirickettsiaceae, as the out-group. 75 Figure 1b shows additionally Thiomicrospira and Hydrogenovibrio strains for which genome 76 sequences are publically available in the Integrated Microbial Genomes (IMG) database, 77 based on the first complete 16S rRNA gene identified in their genome (a full list of Genome 78 IDs is given in Table 2). Figure 2 shows unrooted maximum likelihood trees of amino acid 79 sequences derived from 53-gene concatamers comprised of ribosomal protein genes, 80 concatenated using the ribosomal multilocus sequence typing (rMLST) platform (Jolley et al. 81 2012). Genes used were rpsA through rpsU; rplA through rplF; rplL though rplX, and rpmA 82 through rpmJ genes, with full details and rationale given by Jolley et al., 2012. This latter
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