Complete genome sequence of Granulicella tundricola type strain MP5ACTX9T, an Acidobacteria from tundra soil

DOI:10.4056/sig s.4648353 Standards in Genomic Sciences (2014) 9:449-461 Complete genome sequence of Granulicella tundricola type strain MP5ACTX9T, an Acidobacteria from tundra soil 1 2 3 4 Suman R. Rawat , Minna K. Männistö , Valentin Starovoytov , Lynne Goodwin , Matt 5 6 6 4 5 Nolan Loren Hauser , Miriam Land , Karen Walston Davenport , Tanja Woyke and Max 1 M. Häggblom * 1 Department of Biochemistry and Microbiolog y, Rutgers, The State University of New Jersey, New Brunswick, New Jersey USA 2 Finnish Forest Research Institute, Rovaniemi, Finland 3 Department of Cell Biolog y and Neuroscience, Rutg ers, The State University of New Jersey, Piscataway, New Jersey, USA. 4 Los Alamos National Laboratory, Bioscience Division, Los Alamos, New Mexico, USA 5 DOE Joint Genome Institute, Walnut Creek, California, USA 6 Oak Ridge National Laboratory, Oak Ridg e, Tennessee, USA *Correspondence: Max M Häggblom () Keywords: cold adapted, acidophile, tundra soil, Acidobacteria Granulice lla tundric ola st rain MP5ACTX9 T is a novel species of the g enus Gra nulicella i n subdivision 1 Acidobacteria. G. tundricola is a predomi nant member of soil bacterial communities, active at low temperatures a nd nutrient limiting conditions i n A rctic alpine tundra. The org anism is a cold-a dapted acidophile and a versatile heterot roph t hat hydrolyzes a suite of sug ars and complex polysaccharides. Genome analysis revealed metabolic versatility with g enes involved in metabolism and transport of carbohy drates, including g ene modules encodi ng for the carbohydrate-active enzyme (CAZy) families for the breakdown, utilization and biosy nthesis of diverse structural and st orag e polysaccharides suc h as plant based carbon polymers. The g enome of G. tundric ola st rain MP5ACTX9 T consists of 4, 309,151 bp of a circular chromosome and five meg a plasmids with a total g enome content of 5,503, 984 bp. The g enome comprises 4,705 protein-c odi ng g enes and 52 RNA g enes. Introduction The strain MP5ACTX9T (=ATCC BAA-1859T =DSM 23138T) is the type strain of Granulicella tundricola [tun.dri.co’la. N.L. n. tundra, tundra, a cold treeless region; L. masc. suffix -cola (from L. n. incola) dweller; N.L. n. tundricola tundra dweller] that was isolated from soil at the Malla Nature Reserve, Kilpisjärvi, Finland; 69°01’N, 20°50’E) and described along with other species of the genus Granulicella isolated from tundra soil [1]. Acidobacteria is a phylogenetically and physiologically diverse phylum [2,3], the members of which are ubiquitously found in diverse habitats and are abundant in most soil environments [4,5] including Arctic tundra soils [6,7]. Acidobacteria are rel- atively difficult to cultivate, as they have slow growth rates. To date only subdivisions 1, 3, 4, 8, 10 and 23 Acidobacteria are defined by taxonomically characterized representatives [8-23] as well as three ‘Candidatus’ taxa [24,25]. The phylogenetic diversity, ubiquity and abundance of this group suggest that they play important ecological roles in soils. The abundance of Acidobacteria correlates with soil pH [26,27] and carbon [28,29], with subdivision 1 Acidobacteria being most abundant in slightly acidic soils. Acidobacteria, including members of the genera Granulicella and Terriglobus, dominate the acidic tundra heaths of northern Finland [26,30-32]. Using selective The Genomic Standards Consortium Granulicella tundricola type strain MP5ACTX9T isolation techniques we have been able to isolate several slow growing and fastidious strains of Acidobacteria [1,11]. On the basis of phylogenetic, phenotypic and chemotaxonomic data, including 16S rRNA, rpoB gene sequence similarity and DNA–DNA hybridization, strain MP5ACTX9T was classified as a novel species of the genus Granulicella [1]. Here, we summarize the physiological features together with the complete genome sequence, annotation and data analysis of Granulicella tundricola strain MP5ACTX9T. Classification and features Within the genus Granulicella, eight species are described with validly published names: G. mallensis MP5ACTX8T,G. tundricola MP5ACTX9T, G. arctica MP5ACTX2T,G. sapmiensis S6CTX5AT isolated from Arctic tundra soil [1] and G. paludicola OB1010T, G. paludicola LCBR1, G. pectinivorans TPB6011T ,G. rosea TPO1014T ,G. aggregans TPB6028T isolated from sphagnum peat bogs [2]. Strain MP5ACTX9T shares 95.5 - 97.2% 16S rRNA gene identity with tundra soil strains G. mallensis MP5ACTX8T (95.5%), G. arctica MP5ACTX2T (96.9%), G. sapmiensis S6CTX5AT (97.2%) and 95.2 – 97.7% identity with the sphagnum bog strains, G. pectinivorans TPB6011T (97.7%), G. rosea TPO1014T (97.2%), %), G. aggregans TPB6028T (96.8%), G. paludicola LCBR1 (95.9%), and G. paludicola strain OB1010T (95.3%), which were isolated from sphagnum peat. Phylogenetic analysis based on the 16S rRNA gene of taxonomically classified strains of family Acidobacteriaceae placed G. rosea type strain T4T (AM887759) as the closest taxonomically classified relative of G. tundricola strain MP5ACTX9T (Table 1, Figure 1). Fig ure 1. Phylog enetic tree hig hlig hting the position of G. tundricola MP5ACTX9 T (shown i n bold) relative to the other type strains within subdivision1 Ac idobacteria. The maximum likelihood t ree was inferred f rom 1, 361 alig ned positions of t he 16S rRNA g ene sequences a nd de rived based on t he Tamura-Nei model usi ng MEGA 5 [42]. Bootstrap values >50 (expressed as percentag es of 1,000 replicates) are shown at b ranch points. Bar: 0.01 substitutions per nucleotide position. The corresponding GenBank accession numbers are displayed in parentheses. Strains whose g enomes have been sequenced, a re marke d wit h an asterisk; G. malle nsis MP5AC TX8 T (CP003130), G. tundricola MP5ACTX9T (CP002480), T. saa nensis SP1PR4 T (CP002467), T. roseus KBS63T (CP003379), and A. capsulatum A TCC 51196 T (CP001472). Bryobacter aggre gatus MPL3 (AM 162405) i n SD3 Ac idobacteria was used as an outg roup. 450 Standards in Genomic Sciences Rawat et al. T Table 1. Classification and g eneral features of G. tundric ola strain MP5ACTX9 MIGS ID Property Term Classification Evidence code a Domain Bacteria TAS [33] Phylum Acidobacteria TAS [34,35] Class Acidobacteria TAS [36,37] Order Acidobacteriales TAS [37,38] Family Acidobacteriaceae TAS [35,39] Genus Granulicella TAS [1,40] Species Granulicella tundricola TAS [1] Type strain: MP5ACTX9 (ATCC BAA-1859 = DSM 23138 ) T T T Gram stain negative TAS [1] Cell shape rod TAS [1] Motility non-motile TAS [1] Sporulation not reported NAS Temperature range 4–28°C TAS [1] Optimum temperature 21–24 °C TAS [1] pH range; Optimum 3.5–6.5; 5 TAS [1] Carbon source D-g lucose, maltose, cellobiose, D-fructose, D-galactose, lactose, lactulose, D-mannose, sucrose, trehalose, D-xylose, raffinose, N-acetyl-D-glucosamine, glutamate TAS [1] MIGS-6 Habitat terrestrial, tundra soil TAS [1] MIGS-6.3 Salinity No g rowth w (...truncated)