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Complete Genome Sequence of the Thermophilic Acidobacteria, Pyrinomonas Methylaliphatogenes Type Strain K22T

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Complete Genome Sequence of the Thermophilic Acidobacteria, Pyrinomonas Methylaliphatogenes Type Strain K22T Complete genome sequence of the thermophilic Acidobacteria, Pyrinomonas methylaliphatogenes type strain K22T The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Lee, Kevin C. Y., Xochitl C. Morgan, Jean F. Power, Peter F. Dunfield, Curtis Huttenhower, and Matthew B. Stott. 2015. “Complete genome sequence of the thermophilic Acidobacteria, Pyrinomonas methylaliphatogenes type strain K22T.” Standards in Genomic Sciences 10 (1): 101. doi:10.1186/s40793-015-0099-5. http:// dx.doi.org/10.1186/s40793-015-0099-5. Published Version doi:10.1186/s40793-015-0099-5 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:23845315 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Lee et al. Standards in Genomic Sciences (2015) 10:101 DOI 10.1186/s40793-015-0099-5 EXTENDED GENOME REPORT Open Access Complete genome sequence of the thermophilic Acidobacteria, Pyrinomonas methylaliphatogenes type strain K22T Kevin C. Y. Lee1, Xochitl C. Morgan2,3, Jean F. Power1, Peter F. Dunfield4, Curtis Huttenhower2,3 and Matthew B. Stott1* Abstract Strain K22T isthetypespeciesoftherecently-describedgenusPyrinomonas, in subdivision 4 of the phylum Acidobacteria (Int J Syst Evol Micr. 2014; 64(1):220–7). It was isolated from geothermally-heated soil from Mt. Ngauruhoe, New Zealand, using low-nutrient medium. P. methylaliphatogenes K22T has a chemoheterotrophic metabolism; it can hydrolyze a limited range of simple carbohydrates and polypeptides. Its cell membrane is dominated by iso-branching fatty acids, and up to 40 % of its lipid content is membrane-spanning and ether lipids. It is obligately aerobic, thermophilic, moderately acidophilic, and non-spore-forming. The 3,788,560 bp genome of P. methylaliphatogenes K22T has a G + C content of 59.36 % and contains 3,189 protein-encoding and 55 non-coding RNA genes. Genomic analysis was consistent with nutritional requirements; in particular, the identified transporter classes reflect the oligotrophic nature of this strain. Keywords: Acidobacteria, Pyrinomonas, New Zealand, Thermophile, Soil, Geothermal Introduction particular note is its unusual lipid composition that is Phylotypes from the phylum Acidobacteria1 are commonly dominated by odd-numbered saturated iso-branching detected across a range of ecosystems, including marine fatty acids (iso-C15:0, iso-C17:0, iso-C19:0 and iso-C21:0 that and freshwater bodies, sediments, geothermal systems, and total >88.5 % of the total fatty acid extract) [4]. In soils. Despite the apparent ubiquitous distribution acido- addition, >40 % of the total membrane lipid content is bacterial phyotypes, particularly in soil environments, only made up by iso-branching glycerol ether analogues of the 17 acidobacterial genera (represented by formal description cellular fatty acids and membrane-spanning iso-diabolic and publication of respective type strains, in accordance acids [5]. Membrane-spanning and ether lipids occur ubi- with the International Code of Nomenclature of Prokary- quitously in Archaea, but in recent studies have also been otes [1]) have been validly published [2, 3]. Here we commonly detected in cultivated representatives in sub- present a description of the complete genome sequence division groups 1, 3 and 4 of Acidobacteria [5, 6]. and annotation of Pyrinomonas methylaliphatogenes Subdivision 4 of the Acidobacteria has five validly-named strain K22T (= DSM 25857 = ICMP 18710), the type species: P. methylaliphatogenes K22T,[4] Chloracidobacter- species of the genus Pyrinomonas within subdivision 4 ium thermophilum [7, 8], Blastocatella fastidiosa [9], Aridi- of Acidobacteria. bacter famidurans,andAridibacter kavangonensis [3]. The Pyrinomonas methylaliphatogenes K22T was isolated latter three species are phylogenetically distant from P. from a fumarole on the outer crater rim of the stratovol- methylaliphatogenes K22T, are mesophilic and have differ- cano Mt. Ngauruhoe [4]. It exhibits a Gram-negative cell ing pH ranges and substrate utilization profiles from that of wall, is non-spore-forming, and is catalase- and oxidase- P. methylaliphatogenes K22T. Chloracidobacterium thermo- positive (Table 1). It is a thermophilic and moderately philum is a moderately thermophilic facultatively anoxy- acidophilic obligately aerobic chemoorganotroph. Of genic photoheterotroph isolated from a hotspring microbial mat at Yellowstone National Park [7, 8]. An additional * Correspondence: [email protected] strain, Ellin6075 was isolated from an Australian pasture 1 ō GNS Science, Extremophiles Research Group, Taup , New Zealand soil, and is a mesophilic heterotroph that derives its energy Full list of author information is available at the end of the article © 2015 Lee et al. 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. Lee et al. Standards in Genomic Sciences (2015) 10:101 Page 2 of 8 Table 1 Classification and general features of P. from complex carbohydrate sources, but has little informa- methylaliphatogenes K22T tion available regarding its phenotypic traits [10]. Common MIGS ID Property Term Evidence features shared by subdivision 4 strains include an aerobic a code and heterotrophic phenotype [3, 4], and membrane lipid Current Domain Bacteria TAS [35] iso-diabolic acids [5]. classification Phylum Acidobacteria TAS [36] Class ‘Insertae sedis 99’ Organism information Order ‘Insertae sedis 100’ Classification and features Phylogenetic distances of closest-related phylotypes and Family ‘Insertae sedis 101’ cultivated subdivision 4 acidobacterial strains were deter- Genus Pyrinomonas TAS [4] mined by aligning the representative near full length 16S Species Pyrinomonas TAS [4] rRNA gene sequences (all sequences were > 1,400 nucleo- methylaliphatogenes tides in length) and calculating sequence similarity via a T Type strain K22 (=DSM TAS [4] pair-wise alignment within the ARB software environ- 25857T =ICMP 18710T). ment [11]. Analysis showed that the 16S rRNA gene Gram stain negative TAS [4] sequence of P. methylaliphatogenes K22T (AM749787) is Cell shape rod TAS [4] 85 % similar to B. fastidiosa strain A2-16T (JQ309130), and Motility non-motile TAS [4] is 84 % similar to both A. famidurans strain A22_HD_4HT T Sporulation non-sporulating TAS [4] (KF245634), and A. kavangonensis Ac_23_E3 (KF245633) T Temperature thermophilic (50–69 °C) TAS [4] [3,4,9].Inaddition,P. methylaliphatogenes K22 range shares 85 % 16S rRNA gene sequence similarity with Optimum 65 °C TAS [4] both Ellin6075 (AY234727) [7] and C. thermophilum temperature BT (EF531339) [8]. The most closely-related phylotypes to T pH range moderately acidophilic P. methylaliphatogenes K22 are two sequences from clonal (4.1–7.8) libraries of environmental 16S rRNA genes (EU490264, Optimum pH 6.5 EU490279) retrieved from geothermal soils on Mt. Erebus, Carbon source peptides, proteins, TAS [4] Antarctica [12]; both of these shared 95 % 16S rRNA gene carbohydrates sequence similarity with P. methylaliphatogenes K22T. Terminal electron oxygen TAS [4] Phylogenetic comparison (Fig. 1) showed that P. methylali- receptor phatogenes K22T is a taxonomically-distinct genus and spe- Energy chemoorganotroph TAS [4] cies of subdivision 4 in the phylum Acidobacteria. metabolism Pyrinomonas methylaliphatogenes K22T is non-motile MIGS-6 Habitat geothermal soil TAS [37] and exhibits straight or bent rod cell morphology (0.3 – MIGS-6.3 Salinity non-halophile (no growth TAS [4] 0.6 μm in diameter and 1–4 μm in length) (Fig. 2). It has > 1 % (w/v) NaCl) a temperature range (optimum) for growth of 50–69 °C MIGS-22 Oxygen obligate aerobe TAS [4] (65 °C) and a pH range (optimum) of 4.1–7.8 (6.5). The requirement bacterium has an obligately aerobic metabolism and can MIGS-15 Biotic free-living TAS [4] utilize a small selection of simple carbohydrates includ- relationship ing glucose, lactate, alginate, mannose, xanthan, xylan, MIGS-14 Pathogenicity not reported NAS xylose, arabinose, and sucrose, as well as a limited var- MIGS-4 Geographic Mt Ngauruhoe, TAS [37] iety of proteinaceous substrates including casamino location New Zealand acids, peptone, tryptone, yeast extract and nutrient broth − MIGS-5 Sample 2006 NAS (Table 1). It obtains nitrogen via the uptake of NO3, collection + NH4, urea, yeast extract and casamino acids but cannot MIGS-4.1 Latitude – 39° 9’25.31”S - 175° IDA fix dinitrogen gas. The strain is not able to grow via ’ ” MIGS-4.2 Longitude 38 6.74 E photosynthesis, nor is it able grow autotrophically using MIGS-4.3 Depth not reported IDA CO2 as the sole source of carbon. However, optical dens- MIGS-4.4 Altitude 2,270 m IDA ity of culture is improved via the provision of additional aEvidence codes - IDA inferred from direct assay, TAS traceable author statement CO2 in the headspace during heterotrophic growth,
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