Complete genome sequence of Granulicella mallensis type strain MP5ACTX8T, an acidobacterium from tundra soil
Standards in Genomic Sciences volume 9, pages 71–82 (2013)
Granulicella mallensis MP5ACTX8T is a novel species of the genus Granulicella in subdivision 1of Acidobacteria. G. mallensis is of ecological interest being a member of the dominant soil bacterial community active at low temperatures and nutrient limiting conditions in Arctic alpine tundra. G. mallensis is a cold-adapted acidophile and a versatile heterotroph that hydrolyzes a suite of sugars and complex polysaccharides. Genome analysis revealed metabolic versatility with genes involved in metabolism and transport of carbohydrates. These include gene modules encoding the carbohydrate-active enzyme (CAZyme) family involved in breakdown, utilization and biosynthesis of diverse structural and storage polysaccharides including plant based carbon polymers. The genome of Granulicella mallensis MP5ACTX8T consists of a single replicon of 6,237,577 base pairs (bp) with 4,907 protein-coding genes and 53 RNA genes.
Strain MP5ACTX8T (= ATCC BAA-1857T = DSM 23137T), is the type strain of the species Granulicella mallensis . The genus Granulicella, in subdivision 1 of Acidobacteria, was first described by Pankratov et al. in 2010 . Granulicella mallensis (mal.len′ sis. N. L. fem. adj. mallensis; pertaining to its isolation from soil of Malla Nature Reserve, Kilpisjärvi, Finland; 69°01′N, 20°50′E) was described along with other species of the genus Granulicella isolated from tundra soil  and is one of the two with sequenced genomes, out of eight validly described Granulicella species.
Acidobacteria is one of the most ubiquitous bacterial phyla found in diverse habitats and is abundant in most soil environments [3,4] including Arctic tundra soils [5,6]. Acidobacteria are phylogenetically and physiologically diverse  represented by 26 phylogenetic subdivisions  of which only subdivisions 1, 3, 4, 8, and 10 are defined by taxonomically characterized representatives. To date, subdivision 1 is comprised of eight genera: Acidobacterium , Terriglobus [10,11], Edaphobacter , Granulicella [1,2], Acidipila , Telmatobacter , Acidicapsa  and Bryocella . Subdivision 3, 4 and 10 include only one genus each, namely Bryobacter , Blastocatella  and Thermotomaculum , respectively, while subdivision 8 includes three genera; Holophaga , Geothrix  and Acanthopleuribacter . Three species, ‘Candidatus Koribacter versatilis’ , ‘Candidatus Solibacter usitatus’  and ‘Candidatus Chloracidobacterium thermophilum’  have been described as ‘Candidatus’ taxa. Acidobacteria are relatively difficult to cultivate with slow growth rates and typically require up to several weeks to develop visible colonies on solid media. Nevertheless, the phylogenetic diversity, ubiquity and abundance of this group suggest that they play important ecological roles in soils. The abundance of Acidobacteria has been found to correlate with soil pH [25,26] and carbon [27,28], with subdivision 1 Acidobacteria being most abundant in slightly acidic soils. Our previous studies have shown that Acidobacteria dominate in the acidic tundra heaths of northern Finland [25,29–31]. Using selective 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 MP5ACTX8T was classified as a novel species of the genus Granulicella . Here, we summarize the physiological features together with the complete genome sequence, annotation and data analysis of Granulicella mallensis MP5ACTX8T (Table 1).
Classification and features
Within the genus Granulicella, eight species are described with validly published names: G. mallensis MP5ACTX8T, G. tundricola MP5ACTX9T, G. arctica MP5ACTX2T and G. sapmiensis S6CTX5AT isolated from Arctic tundra soil  and G. paludicola OB1010T, G. pectinivorans TPB6011T, G. rosea TPO1014T and G. aggregans TPB6028T isolated from sphagnum peat bogs . Strain MP5ACTX8T showed 95.5–96.1% 16S rRNA gene sequence identity to tundra soil strains, G. tundricola MP5ACTX9T (95.5%), G. sapmiensis S6CTX5AT (96.2%) and G. arctica MP5ACTX2T (96.1%) and 94.6–97.4% to G. rosea TPO1014T (94.6%), G. aggregans TPB6028T (96.0%), G. pectinivorans TPB6011T (96.1%), G. paludicola OB1010T (96.5%) and G. paludicola LCBR1 (97.4%). Phylogenetic analysis based on the 16S rRNA gene of taxonomically classified strains of family Acidobacteriaceae placed G. paludicola type strain OB1010 T as the closest taxonomically classified relative of G. mallensis MP5ACTX8T (Figure 1).
Morphology and physiology
G. mallensis grows on R2 medium (Difco) at pH 3.5–6.5 (optimum pH 5) and at +4 to +28 °C (optimum 24–27 °C) . On R2 agar, strain MP5ACTX8T forms opaque white mucoid colonies with a diameter of approximately 1 mm. Cells are Gram-negative, non-motile, aerobic rods, approximately 0.5–0.7 mm wide and 0.6–1.3 mm long. Growth observed with up to 1.5% NaCl (w/v) (Table 1). The cell-wall structure in ultrathin sections of electron micrographs of cells of MP5ACTX8T is shown in Figure 2.
G. mallensis utilizes D-glucose, maltose, cellobiose, D-fructose, D-galactose, lactose, lactulose, D-mannose, D-ribose, raffinose, sucrose, trehalose, D-xylose, N-acetyl-D-glucosamine, glucuronate, glutamate, melezitose and salicin, but does not utilize D-arabinose, acetate, formate, pyruvate, malate, mannitol, D- or L-alanine, D-glycine, L-leucine, L-ornithine, gluconic acid, aspartate, dulcitol, butyrate, caproate, valerate, lactate, oxalate, propionate, fumarate, adonitol, methanol, ethanol, succinate, D-sorbitol or myoinositol, when grown using VL55 mineral medium with 100 mg yeast extract l−1. G. mallensis hydrolyzes aesculin, starch, pectin, laminarin and lichenan, but not gelatin, cellulose, xylan, sodium alginate, pullulan, chitosan or chitin on R2 medium. Strains show positive reaction for acid and alkaline phosphatases, leucine arylamidase, a-chymotrypsin, naphthol-AS-BI-phosphohydrolase, α- and β-galactosidases, α- and β-glucosidases, N-acetyl-β-glucosaminidase, β-glucuronidase, trypsin and valine arylamidase, but negative for α-fucosidase, α-mannosidase, esterase (C4 and C8), lipase (C14) and cystine arylamidase. Strain MP5ACTX8T reduces nitrate to nitrite. Strain MP5ACTX8T is resistant to the antibiotics erythromycin, chloramphenicol, neomycin, rifampicin, streptomycin, gentamicin, polymyxin B and penicillin, but susceptible to ampicillin, kanamycin, tetracycline, lincomycin, novobiocin and bacitracin .
The major cellular fatty acids in G. mallensis are iso-C15:0 (45.3%), C16:1ω7c (28.7%), iso-C13:0 (8.3%) and C16:0 (8.9%). The cellular fatty acid compositions of strain MP5ACTX8T were relatively similar to that of other Granulicella strains with fatty acids iso-C15:0 and C16:1ω7c being most abundant in all strains. Strain MP5ACTX8T contains MK-8 as the major quinone.
Genome sequencing and annotation
Genome project history
G. mallensis strain MP5ACTX8T was selected for sequencing in 2009 by the DOE Joint Genome Institute (JGI) community sequencing program. The Quality Draft (QD) assembly and annotation were completed on December 26, 2010. The complete genome was made available on Dec. 1, 2011. The genome project is deposited in the Genomes On-Line Database (GOLD)  and the complete genome sequence of strain MP5ACTX8T is deposited in GenBank (CP003130). Table 2 presents the project information and its association with MIGS version 2.0 .
Growth conditions and genomic DNA extraction
G. mallensis MP5ACTX8T was cultivated on R2 medium as previously described . Genomic DNA (gDNA) of high sequencing quality was isolated using a modified CTAB method and evaluated according to the Quality Control (QC) guidelines provided by the DOE Joint Genome Institute .
Genome sequencing and assembly
The finished genome of G. mallensis MP5ACTX8T (JGI ID 4088692) was generated at the DOE Joint genome Institute (JGI) using a combination of Illumina  and 454 technologies . For this genome, an Illumina GAii shotgun library which generated 59,701,420 reads totaling 4537.3 Mb, a 454 Titanium standard library which generated 136,708 reads and a paired end 454 library with an average insert size of 10.3 kb which generated 157,336 reads totaling 172.0 Mb of 454 data, were constructed and sequenced. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI website . The 454 Titanium standard data and the 454 paired end data were assembled with Newbler, version 2.3. Illumina sequencing data was assembled with Velvet, version 0.7.63 . The 454 Newbler consensus shreds, the Illumina Velvet consensus shreds and the read pairs in the 454 paired end library were integrated using parallel phrap, version SPS - 4.24 (High Performance Software, LLC) . The software Consed  was used in the finishing process. The Phred/Phrap/Consed software package  was used for sequence assembly and quality assessment in the subsequent finishing process. Illumina data was used to correct potential base errors and increase consensus quality using the software Polisher developed at JGI (Alla Lapidus, unpublished). Possible misassemblies were corrected using gapResolution (Cliff Han, un-published), Dupfinisher  or sequencing cloned bridging PCR fragments with sub-cloning. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR (J-F Cheng, unpublished) primer walks. The final assembly is based on 74.2 Mb of 454 data which provides an average 18.5× coverage and 1318.5 Mb of Illumina data which provides an average 213× coverage of the genome.
Genes were identified using Prodigal  as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline . The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) non-redundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COGs [53,54], and InterPro. These data sources were combined to assert a product description for each predicted protein. Non-coding genes and miscellaneous features were predicted using tRNAscan-SE , RNAMMer , Rfam , TMHMM , and signalP . Additional gene prediction analysis and functional annotation were performed within the Integrated Microbial Genomes Expert Review (IMG-ER) platform .
The genome consists of one circular chromosome of 6,211,694 bp in size with a GC content of 57.8 mol% and consists of 53 RNA genes (Figure 3 and Table 3). Of the 4,960 predicted genes, 4,907 are protein-coding genes (CDSs) and 90 are pseudogenes. Of the total CDSs, 70.5% represent COG functional categories and 16% consist of signal peptides. The distribution of genes into COG functional categories is presented in Figure 3 and Table 4.
Granulicella mallensis type strain MP5ACTX8T has the largest genome size of 6.2 Mbp. among the three tundra soil strains of subdivision 1 Acidobacteria . Genome analysis of Granulicella mallensis identified a high abundance of genes assigned to COG functional categories for transport and metabolism of carbohydrates (9.1%) and amino acids (6.7%) and involved in cell envelope biogenesis (8.3%) and transcription (8.6%). Further genome analysis revealed an abundance of gene modules encoding for functional activities within the carbohydrate-active enzymes (CAZy) family  involved in breakdown, utilization and biosynthesis of carbohydrates. G. mallensis hydrolyzed complex carbon polymers, including CMC, pectin, lichenin, laminarin and starch, and utilized sugars such as cellobiose, D-mannose, D-xylose, D-trehalose. This parallels genome predictions for CDSs encoding for enzymes such as cellulases, pectinases, alginate lyases, trehalase and amylases. In addition, the G. mallensis genome contained a cluster of genes in the neighborhood of the cellulose synthase gene (bcsAB) which included cellulase (bscZ) (endoglucanase Y) of family GH8, cellulose synthase operon protein (bcsC) and a cellulose synthase operon protein (yhjQ) involved in cellulose biosynthesis. Detailed comparative genome analysis of G. mallensis MP5ACTX8T with other Acidobacteria strains for which finished genomes were available is reported in Rawat et al. . The data thus suggests that G. mallensis is involved in hydrolysis, the utilization of stored carbohydrates, and in the biosynthesis of exopolysaccharides from organic matter and plant based polymers in the soil. Therefore, we infer that strain G. mallensis may be central to carbon cycling processes in arctic and boreal soil ecosystems.
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The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy Under Contract No. DE-AC02-05CH11231. This work was funded in part by the Academy of Finland and the New Jersey Agricultural Experiment Station.
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Rawat, S.R., Männistö, M.K., Starovoytov, V. et al. Complete genome sequence of Granulicella mallensis type strain MP5ACTX8T, an acidobacterium from tundra soil. Stand in Genomic Sci 9, 71–82 (2013). https://doi.org/10.4056/sigs.4328031
- cold adapted
- tundra soil