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Bacillus Ferrooxidans Sp. Nov., an Iron(II)-Oxidizing Bacterium Isolated from Paddy Soil§

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Bacillus Ferrooxidans Sp. Nov., an Iron(II)-Oxidizing Bacterium Isolated from Paddy Soil§ Journal of Microbiology (2018) Vol. 56, No. 7, pp. 472–477 eISSN 1976-3794 DOI 10.1007/s12275-018-7543-3 pISSN 1225-8873 Bacillus ferrooxidans sp. nov., an iron(II)-oxidizing bacterium isolated from paddy soil§ Introduction Guo-Wei Zhou1,2, Xiao-Ru Yang2*, Jian-Qiang Su2, Bang-Xiao Zheng2,3, 1,2 Nitrate-dependent iron(II) oxidation significantly contributes and Yong-Guan Zhu to iron cycling in pH-neutral anoxic zones in sediments or terrestrial environments (Ratering and Schnell, 2001; Aka- 1State Key Lab of Urban and Regional Ecology, Research Center for saka, 2003). The majority of identified anaerobic nitrate- Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing reducing iron(II) oxidizers are affiliated to Proteobacteria 100085, P. R. China 2Key Lab of Urban Environment and Health, Institute of Urban (Hedrich et al., 2011). It has been reported that Fe(II) oxida- Environment, Chinese Academy of Sciences, Xiamen 361021, P. R. China tion is mediated by nitrate-reducing bacteria, where nitrite 3University of Chinese Academy of Sciences, Beijing 100049, P. R. China could act as a potent chemical oxidant for Fe(II) (Carlson et al., 2013). Bacillus spp. have been reported with denitrifica- (Received Dec 13, 2017 / Revised Apr 25, 2018 / Accepted May 3, 2018) tion under both aerobic and anaerobic conditions (Pichinoty et al., 1979; Ma et al., 2000; Yu et al., 2005). Bacillus species An endospore-forming bacterium, designated YT-3T, was are endospore-forming aerobic or facultatively anaerobic isolated from a paddy soil in Yingtan, Jiangxi, China. Cells of bacteria, and a considerable number of Bacillus strains are strain YT-3T were Gram-positive, rod-shaped, facultative capable of reducing nitrate to nitrite (Verbaendert et al., anaerobic, catalase, and oxidase positive. The optimum growth 2011). Bacillus are ubiquitous in various environments, in- temperature and pH were 30°C (ranged from 15 to 50°C) cluding soil, water and air. Thus, the potential contribution and 6.5–7.0 (ranged from 3 to 11), respectively. Analysis of of Bacillus spp. to Fe(II) oxidation should not be ignored. the 16S rRNA gene sequence showed that strain YT-3T was Bacillus spp. have been identified to be involved in iron(II) affiliated to the genus Bacillus and displayed the highest si- oxidation in paddy soil, where seasonal flooding can pro- milarity to that of Bacillus drentensis JCM 21707T (98.3%), vide an anoxic compartment for nitrate-dependent iron(II) followed by B. ginsengisoli JCM 17335T (97.8%) and B. fu- oxidizers (Ratering and Schnell, 2001; Akasaka, 2003; Sun- marioli JCM 21708T (97.0%). The similarity of rpoB gene daram et al., 2012). Bacteria in this genus are Gram-posi- sequence between strain YT-3T and B. drentensis JCM 21707T, tive, menaquinone-7-producing, and contain iso- and an- B. ginsengisoli JCM 17335T and B. fumarioli JCM 21708T was teiso-saturated fatty acids as major components of lipid acids 80.4%, 81.5%, and 82.1%, respectively. The genomic DNA (Weber et al., 2001; Berenjian et al., 2012). In this study, G + C content was 44.9 mol%. The predominant respiratory the strain YT-3T was isolated from paddy soil with the ability quinone was Menaquinone-7, and meso-diaminopimelic acid of iron(II) oxidation and was suggested as a novel species was present in the peptidoglycan layer of cell wall. The ma- in the genus Bacillus. jor fatty acids were C15:0 anteiso (36.2%), C14:0 iso (19.6%), C15:0 iso (17.4%), and C16:0 iso (9.8%). The polar lipid pro- file consisted of diphosphatidylglycerol, phosphatidyletha- Materials and Methods nolamine, phosphatidylglycerol, phospholipids, and am- moniac phospholipids. The DNA-DNA hybridization values Isolation and culture conditions between isolate YT-3T and B. drentensis (JCM 21707T), B. T T Paddy soil sample was collected from Yingtan, Jiangxi, China ginsengisoli (JCM 17335 ), and B. fumarioli (JCM 21708 ) (116°82�GE, 28°2�GN). The soil is a typical red soil with abun- were 36.3%, 30.3%, and 25.3%, respectively. On the basis of T dant Fe(III) (oxyhydr) oxide in southern China. To isolate physiological, genetic and biochemical data, strain YT-3 ferrous iron-oxidizing bacteria (FeOB), soil slurry was pre- represented a novel species of the genus Bacillus, for which pared by suspending 3 g soil in 50 ml anoxic distilled water the name Bacillus ferrooxidans sp. nov was proposed. The type T T T and shaking at 120 rpm for 2 h at 25°C. Enrichment of FeOB strain is YT-3 (= KCTC 33875 = CCTCC AB 2017049 ). was initiated by inoculation of 2 ml well-mixed slurry into 50 ml serum vials (with 20 ml sterilized and anoxic FeOB Keywords: Bacillus ferrooxidans, novel species, iron(II)-oxi- medium) and followed by incubation at 25°C in the dark dizing bacteria, polyphasic taxonomy, paddy soil without shaking. The FeOB medium (pH 6.8–7.2) contained MgSO4·7H2O (0.5 g/L), CaCl2·H2O (0.1 g/L), NH4Cl (0.3 g/L), *For correspondence. E-mail: [email protected]; Tel.: +86-592-6190997; KH2PO4 (0.6 g/L), 1 ml/L vitamin solution, 1 ml/L trace el- Fax: +86-592-6190977 §Supplemental material for this article may be found at ement solution SL10, 1 ml/L selenite-tungstate solution, 22 http://www.springerlink.com/content/120956. mmol/L bicarbonate buffer, FeCl2 (10 mmol/L) and NaNO3 Copyright G2018, The Microbiological Society of Korea (10 mmol/L) (Klueglein and Kappler, 2013; Klueglein et al., Bacillus ferrooxidans sp. nov. 473 (A) (B) (C) Fig. 1. Scanning electron microscopic imaging of the strain YT-3T after 2-day growth on R2A plates at 30°C in the anaerobic box. (D) (E) (F) 2015). Stock solutions of the trace element solution, element Phylogenetic analysis solution SL10, selenite-tungstate solution and FeCl were 2 Genomic DNA was extracted using a FastDNA Spin kit (MP prepared as described previously and were filtered through Biomedical). The 16S rRNA genes of strain YT-3T and the 0.22 μm filter (Klueglein and Kappler, 2013; Klueglein et closely related reference type strains including B. drentensis al., 2015). The medium was purged with N /CO (80/20%) T T 2 2 JCM 21707 , B. ginsengisoli JCM 17335 , and B. fumarioli to deplete oxygen. Fe(II) oxidation was indicated when the JCM 21708T, were amplified using universal primers (27F medium became brick-red after the FeOB enrichment was and 1492R) (Baker et al., 2003). Sequences closely related to transferred (10%) to fresh media for four generations. To T 16S rRNA genes of strain YT-3 were retrieved from the Ez- isolate the FeOB, the enrichment was 10-fold serially di- -3 Taxon server (http://www.ezbiocloud.net/eztaxon) and aligned luted to 10 and 10 μl of each dilution was spread on the using CLUSTAL X (Wang et al., 2012), and a phylogenetic FeOB medium agar plates (2%; w/v). The isolation proce- tree was generated with MEGA 5.0 based on neighbor-join- dure and incubation were conducted in an anaerobic glove- ing, minimum-evolution and maximum-likelihood methods box (N2:CO2:H2 = 90:5:5) (Shel Lab Bactron) equipped with (bootstrap values, 1,000 replications) (Felsenstein, 1985; Lar- a portable oxygen concentration detector. Strain YT-3T was kin et al., 2007; Tamura et al., 2013). The housekeeping gene one of the colonies on the FeOB medium plates. Individual rpoB of strain YT-3T and reference type strains were ampli- colonies were streaked onto fresh FeOB agar plates at least fied using primers (BA-rpoBF: GACGATCATYTWGGAAA three times for purification before subsequent identification. CCG; BA-rpoBR: GGNGTYTCRATYGGACACAT) (Ko et Pure colonies were maintained in R2A broth with 20% gly- al., 2004). cerol and stored at -80°C. Reference strains, B. drentensis T T The GenBank accession number for the 16S rRNA gene se- (JCM 21707 ), B. ginsengisoli (JCM 17335 ), and B. fumarioli T T quence of strain YT-3 is KY628809. The accession numbers (JCM 21708 ), were purchased from the Japan Collection for the rpoB gene sequence of YT-3T, B. ferrooxidans, B. dren- of Microorganisms (JCM). Fig. 2. Neighbor-joining phylogenetic tree (500 bootstraps) of 16S rRNA gene se- quences indicating the phylogenetic posi- tion of the strain YT-3T among the related species. Filled circles indicate that the cor- responding nodes are recovered in the tree generated with maximum-likelihood and minimum-evolution methods. Bar repre- sents 2 nucleotide substitutions per 100 nu- cleotide positions. Bootstrap values above 70% are given at the node. The sequence of Escherichia coli that affiliated to the γ-Pro- teobacteria was used as the outgroup. 474 Zhou et al. tensis (JCM 21707T), B. ginsengisoli (JCM 17335T) and B. Chemotaxonomic and genomic analysis T fumarioli (JCM 21708 ) were SRX3964264, SRX3940797, The amino acids in the cell wall were analyzed using thin SRX3940794, and SRX3940796, respectively. layer chromatography (TLC) (Staneck and Roberts, 1974). Genomic DNA G + C contents were determined by reversed- Phenotypic analysis phase high-performance liquid-chromatography (RP-HPLC) Colony morphology was observed after aerobic growth on (Shin and Kahng, 2017). DNA-DNA hybridization was an- R2A agar plates for 48 h at 30°C using the Lab-RAM Aramis alyzed in triplicate using an ultra violet/visible (UV/VIS) spec- Horiba Jobin Yvon Confocal Raman microscope (Horiba trophotometer (Lambda 35 ES, Perkin Elmer). DNA-DNA Jobin Yvon) with an integrated Olympus BXFM microscope. relatedness values were shown as a mean of the three dif- Cell size and shape were measured using Scanning Electron ferent replicates (mean ± SD). The fatty acids of the strain Microscopy (SEM) (S-4800, Hitachi). The Gram reaction YT-3T and the reference type strains were extracted after of the strain was tested by using the 3% KOH method (Buck, growth in R2A medium at 30°C for 3 days by using a stan- 1982).
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