Genome Analysis Coupled with Physiological Studies Reveals a Diverse Nitrogen Metabolism in Methylocystis sp. Strain SC2

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Dam, Bomba ^a,b,d   Dam, Somasri ^a,b,e   Blom, Jochen ^c   Liesack, Werner ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

^d VISVA BHARATI UNIVERSITY   (India)

^e VIDYASAGAR UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; NITROGEN; NITROUS OXIDE REDUCTASE; OXYGEN;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; CHROMOSOME; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DENITRIFICATION; GAMMAPROTEOBACTERIA; GENOME ANALYSIS; METHYLOCYSTACEAE; METHYLOCYSTIS; METHYLOSINUS TRICHOSPORIUM; NITROGEN FIXATION; NITROGEN METABOLISM; NONHUMAN; NOS GENE; OPERON; PHYLOGENY; PLASMID; SEQUENCE HOMOLOGY; VERRUCOMICROBIA;

BASE SEQUENCE; GENOME, BACTERIAL; METHYLOCYSTACEAE; MOLECULAR SEQUENCE DATA; NITROGEN; PHYLOGENY;

EID: 84885395730     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074767     Document Type: Article

References (119)

1. Hanson RS, Hanson TE, (1996) Methanotrophic bacteria. Microbiol Rev 60: 439-471.
2. Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, et al. (2009) Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 1: 293-306.
3. Eller G, Frenzel P, (2001) Changes in activity and community structure of methane-oxidizing bacteria over the growth period of rice. Appl Environ Microbiol 67: 2395-2403.
4. Horz HP, Yimga MT, Liesack W, (2001) Detection of methanotroph diversity on roots of submerged rice plants by molecular retrieval of pmoA, mmoX, mxaF, and 16S rRNA and ribosomal DNA, including pmoA-based terminal restriction fragment length polymorphism profiling. Appl Environ Microbiol 67: 4177-4185.
5. Radajewski S, Webster G, Reay DS, Morris SA, Ineson P, et al. (2002) Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148: 2331-2342.
6. Knief C, Lipski A, Dunfield PF, (2003) Diversity and activity of methanotrophic bacteria in different upland soils. Appl Environ Microbiol 69: 6703-6714.
7. Knief C, Kolb S, Bodelier PL, Lipski A, Dunfield PF, (2006) The active methanotrophic community in hydromorphic soils changes in response to changing methane concentration. Environ Microbiol 8: 321-333.
8. Chen Y, Dumont MG, Cebron A, Murrell JC, (2007) Identification of active methanotrophs in a landfill cover soil through detection of expression of 16S rRNA and functional genes. Environ Microbiol 9: 2855-2869.
9. Cebron A, Bodrossy L, Chen Y, Singer AC, Thompson IP, et al. (2007) Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol Ecol 62: 12-23.
10. McDonald IR, Murrell JC, (1997) The particulate methane monooxygenase gene pmoA and its use as a functional gene probe for methanotrophs. FEMS Microbiol Lett 156: 205-210.
11. Dedysh SN, Dunfield PF, Derakshani M, Stubner S, Heyer J, et al. (2003) Differential detection of type II methanotrophic bacteria in acidic peatlands using newly developed 16S rRNA-targeted fluorescent oligonucleotide probes. FEMS Microbiol Ecol 43: 299-308.
12. Chen Y, Dumont MG, McNamara NP, Chamberlain PM, Bodrossy L, et al. (2008) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ Microbiol 10: 446-459.
13. Nauer PA, Dam B, Liesack W, Zeyer J, Schroth MH, (2012) Activity and diversity of methane-oxidizing bacteria in glacier forefields on siliceous and calcareous bedrock. Biogeosciences 9: 2259-2274.
14. Belova SE, Baani M, Suzina NE, Bodelier PLE, Liesack W, et al. (2011) Acetate utilization as a survival strategy of peat-inhabiting Methylocystis spp. Environ Microbiol Rep 3: 36-46.
15. Im J, Lee S-W, Yoon S, DiSpirito AA, Semrau JD, (2011) Characterization of a novel facultative Methylocystis species capable of growth on methane, acetate and ethanol. Environ Microbiol Rep 3: 174-181.
16. Nyerges G, Han SK, Stein LY, (2010) Effects of ammonium and nitrite on growth and competitive fitness of cultivated methanotrophic bacteria. Appl Environ Microbiol 76: 5648-5651.
17. Nyerges G, Stein LY, (2009) Ammonia cometabolism and product inhibition vary considerably among species of methanotrophic bacteria. FEMS Microbiol Lett 297: 131-136.
18. Ricke P, Erkel C, Kube M, Reinhardt R, Liesack W, (2004) Comparative analysis of the conventional and novel pmo (particulate methane monooxygenase) operons from Methylocystis strain SC2. Appl Environ Microbiol 70: 3055-3063.
19. Baani M, Liesack W, (2008) Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2. Proc Natl Acad Sci USA 105: 10203-10208.
20. Dam B, Dam S, Kube M, Reinhardt R, Liesack W, (2012) Complete genome sequence of Methylocystis sp. strain SC2, an aerobic methanotroph with high-affinity methane oxidation potential. J Bacteriol 194: 6008-6009.
21. Murrell JC, Dalton H, (1983) Nitrogen fixation in obligate methanotrophs. J Gen Microbiol 129: 3481-3486.
22. Dedysh SN, Ricke P, Liesack W, (2004) NifH and NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria. Microbiology 150: 1301-1313.
23. Auman AJ, Speake CC, Lidstrom ME, (2001) nifH sequences and nitrogen fixation in type I and type II methanotrophs. Appl Environ Microbiol 67: 4009-4016.
24. Khadem AF, Pol A, Jetten MS, Op den Camp HJ, (2010) Nitrogen fixation by the verrucomicrobial methanotroph 'Methylacidiphilum fumariolicum' SolV. Microbiology 156: 1052-1059.
25. Zumft WG, (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533-616.
26. Waibel AE, Peter T, Carslaw KS, Oelhaf H, Wetzel G, et al. (1999) Arctic ozone loss due to denitrification. Science 283: 2064-2069.
27. Klotz MG, Stein LY, (2008) Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiol Lett 278: 146-156.
28. Wrage N, Velthof GL, van Beusichem ML, Oenema O, (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33: 1723-1732.
29. Campbell MA, Nyerges G, Kozlowski JA, Poret-Peterson AT, Stein LY, et al. (2011) Model of the molecular basis for hydroxylamine oxidation and nitrous oxide production in methanotrophic bacteria. FEMS Microbiol Lett 322: 82-89.
30. Bergmann DJ, Zahn JA, Hooper AB, DiSpirito AA, (1998) Cytochrome P460 genes from the methanotroph Methylococcus capsulatus Bath. J Bacteriol 180: 6440-6445.
31. Elmore BO, Bergmann DJ, Klotz MG, Hooper AB, (2007) Cytochromes P460 and c′-beta; a new family of high-spin cytochromes c. FEBS Lett 581: 911-916.
32. Poret-Peterson AT, Graham JE, Gulledge J, Klotz MG, (2008) Transcription of nitrification genes by the methane-oxidizing bacterium, Methylococcus capsulatus strain Bath. ISME J 2: 1213-1220.
33. Sutka RL, Ostrom NE, Ostrom PH, Gandhi H, Breznak JA, (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun Mass Spectrom 17: 738-745.
34. Sutka RL, Ostrom NE, Ostrom PH, Breznak JA, Gandhi H, et al. (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microbiol 72: 638-644.
35. Stein LY, Klotz MG, (2011) Nitrifying and denitrifying pathways of methanotrophic bacteria. Biochem Soc Trans 39: 1826-1831.
36. Stein LY, (2011) Surveying N2O-producing pathways in bacteria. Methods Enzymol 486: 131-152.
37. Arp DJ, Stein LY, (2003) Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Crit Rev Biochem Mol Biol 38: 471-495.
38. Zahn JA, Duncan C, DiSpirito AA, (1994) Oxidation of hydroxylamine by cytochrome P-460 of the obligate methylotroph Methylococcus capsulatus Bath. J Bacteriol 176: 5879-5887.
39. Stein LY, Yoon S, Semrau JD, Dispirito AA, Crombie A, et al. (2010) Genome sequence of the obligate methanotroph Methylosinus trichosporium strain OB3b. J Bacteriol 192: 6497-6498.
40. del Cerro C, Garcia JM, Rojas A, Tortajada M, Ramon D, et al. (2012) Genome sequence of the methanotrophic poly-beta-hydroxybutyrate producer Methylocystis parvus OBBP. J Bacteriol 194: 5709-5710.
41. Stein LY, Bringel F, DiSpirito AA, Han S, Jetten MS, et al. (2011) Genome sequence of the methanotrophic alphaproteobacterium Methylocystis sp. strain Rockwell (ATCC 49242). J Bacteriol 193: 2668-2669.
42. Chen Y, Crombie A, Rahman MT, Dedysh SN, Liesack W, et al. (2010) Complete genome sequence of the aerobic facultative methanotroph Methylocella silvestris BL2. J Bacteriol 192: 3840-3841.
43. Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H, et al. (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2: e303.
44. Kits KD, Kalyuzhnaya MG, Klotz MG, Jetten MS, Op den Camp HJ, et al. (2013) Genome sequence of the obligate gammaproteobacterial methanotroph Methylomicrobium album strain BG8. Genome Announc 1: e00170-13.
45. Vuilleumier S, Khmelenina VN, Bringel F, Reshetnikov AS, Lajus A, et al. (2012) Genome sequence of the haloalkaliphilic methanotrophic bacterium Methylomicrobium alcaliphilum 20Z. J Bacteriol 194: 551-552.
46. Boden R, Cunliffe M, Scanlan J, Moussard H, Kits KD, et al. (2011) Complete genome sequence of the aerobic marine methanotroph Methylomonas methanica MC09. J Bacteriol 193: 7001-7002.
47. Svenning MM, Hestnes AG, Wartiainen I, Stein LY, Klotz MG, et al. (2011) Genome sequence of the Arctic methanotroph Methylobacter tundripaludum SV96. J Bacteriol 193: 6418-6419.
48. Hou S, Makarova KS, Saw JH, Senin P, Ly BV, et al. (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3: 26.
49. Khadem AF, Wieczorek AS, Pol A, Vuilleumier S, Harhangi HR, et al. (2012) Draft genome sequence of the volcano-inhabiting thermoacidophilic methanotroph Methylacidiphilum fumariolicum strain SolV. J Bacteriol 194: 3729-3730.
50. Dam B, Kube M, Dam S, Reinhardt R, Liesack W, (2012) Complete sequence analysis of two methanotroph-specific repABC-containing plasmids from Methylocystis sp. strain SC2. Appl Environ Microbiol 78: 4373-4379.
51. Kolsto AB, (1997) Dynamic bacterial genome organization. Mol Microbiol 24: 241-248.
52. Lima-Mendez G, Van Helden J, Toussaint A, Leplae R, (2008) Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 24: 863-865.
53. Makarova KS, Grishin NV, Koonin EV, (2006) The HicAB cassette, a putative novel, RNA-targeting toxin-antitoxin system in archaea and bacteria. Bioinformatics 22: 2581-2584.
54. Yamaguchi Y, Park JH, Inouye M, (2011) Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45: 61-79.
55. Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K, et al. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112: 131-140.
56. Zhang Y, Zhang J, Hara H, Kato I, Inouye M, (2005) Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J Biol Chem 280: 3143-3150.
57. Kamada K, Hanaoka F, (2005) Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Mol Cell 19: 497-509.
58. Maisonneuve E, Shakespeare LJ, Jørgensen MG, Gerdes K, (2011) Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A 108: 13206-13211.
59. Kolodkin-Gal I, Engelberg-Kulka H, (2006) Induction of Escherichia coli chromosomal mazEF by stressful conditions causes an irreversible loss of viability. J Bacteriol 188: 3420-3423.
60. Hazan R, Sat B, Engelberg-Kulka H, (2004) Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J Bacteriol 186: 3663-3669.
61. Grissa I, Vergnaud G, Pourcel C, (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35: W52-57.
62. Grissa I, Vergnaud G, Pourcel C, (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172.
63. Barrangou R, Horvath P, (2012) CRISPR: New horizons in phage resistance and strain identification. Annu Rev Food Sci Technol 3: 143-162.
64. Deveau H, Garneau JE, Moineau S, (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64: 475-493.
65. Horvath P, Barrangou R, (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170.
66. Palmer KL, Gilmore MS, (2010) Multidrug-resistant enterococci lack CRISPR-cas. MBio 1(4): e00227-10.
67. Horvath P, Coute-Monvoisin AC, Romero DA, Boyaval P, Fremaux C, et al. (2009) Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int J Food Microbiol 131: 62-70.
68. Gao F, Zhang CT, (2008) Ori-Finder: a web-based system for finding oriCs in unannotated bacterial genomes. BMC Bioinformatics 9: 79.
69. Sernova NV, Gelfand MS, (2008) Identification of replication origins in prokaryotic genomes. Brief Bioinform 9: 376-391.
70. Hendrickson H, Lawrence JG, (2007) Mutational bias suggests that replication termination occurs near the dif site, not at Ter sites. Mol Microbiol 64: 42-56.
71. Kono N, Arakawa K, Tomita M, (2011) Comprehensive prediction of chromosome dimer resolution sites in bacterial genomes. BMC Genomics 12: 19.
72. Garcia-Martinez J, Bescos I, Rodriguez-Sala JJ, Rodriguez-Valera F, (2001) RISSC: a novel database for ribosomal 16S-23S RNA genes spacer regions. Nucleic Acids Res 29: 178-180.
73. Nomura M, Morgan EA, (1977) Genetics of bacterial ribosomes. Annu Rev Genet 11: 297-347.
74. Matsugi J, Murao K, (2004) Genomic investigation of the system for selenocysteine incorporation in the bacterial domain. Biochim Biophys Acta 1676: 23-32.
75. Akiyama Y, Ito K, (2003) Reconstitution of membrane proteolysis by FtsH. J Biol Chem 278: 18146-18153.
76. Akiyama Y, (2009) Quality control of cytoplasmic membrane proteins in Escherichia coli. J Biochem 146: 449-454.
77. Ito K, Akiyama Y, (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59: 211-231.
78. Holmes AJ, Costello A, Lidstrom ME, Murrell JC, (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132: 203-208.
79. Semrau JD, Chistoserdov A, Lebron J, Costello A, Davagnino J, et al. (1995) Particulate methane monooxygenase genes in methanotrophs. J Bacteriol 177: 3071-3079.
80. Bedard C, Knowles R, (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4+, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53: 68-84.
81. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, et al. (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A 109: 19709-19714.
82. Buurman ET, Teixeira de Mattos MJ, Neijssel OM, (1991) Futile cycling of ammonium ions via the high affinity potassium uptake system (Kdp) of Escherichia coli. Arch Microbiol 155: 391-395.
83. Merrick MJ, Edwards RA, (1995) Nitrogen control in bacteria. Microbiol Rev 59: 604-622.
84. Helling RB, (1998) Pathway choice in glutamate synthesis in Escherichia coli. J Bacteriol 180: 4571-4575.
85. Kohler T, Harayama S, Ramos JL, Timmis KN, (1989) Involvement of Pseudomonas putida RpoN sigma factor in regulation of various metabolic functions. J Bacteriol 171: 4326-4333.
86. Weiss V, Kramer G, Dunnebier T, Flotho A, (2002) Mechanism of regulation of the bifunctional histidine kinase NtrB in Escherichia coli. J Mol Microbiol Biotechnol 4: 229-233.
87. Pawlowski K, Klosse U, de Bruijn FJ, (1991) Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Mol Gen Genet 231: 124-138.
88. Takeda K, (1988) Characteristics of a nitrogen-fixing methanotroph, Methylocystis T-1. Antonie van Leeuwenhoek 54: 521-534.
89. Dedysh SN, Khmelenina VN, Suzina NE, Trotsenko YA, Semrau JD, et al. (2002) Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int J Syst Evol Microbiol 52: 251-261.
90. Dalton H, Whittenbury R, (1976) The acetylene reduction technique as an assay for nitrogenase activity in the methane oxidizing bacterium Methylococcus capsulatus strain Bath. Arch Microbiol 109: 147-151.
91. De Bont JAM, Mulder EG, (1974) Nitrogen fixation and co-oxidation of ethylene by a methane-utilizing bacterium. J Gen Microbiol 83: 113-121.
92. Zhivotchenko AG, Nikonova ES, Jørgensen MH, (1995) Effect of fermentation conditions on N2 fixation by Methylococcus capsulatus. Bioprocess Biosyst Eng 14: 9-15.
93. Ren T, Roy R, Knowles R, (2000) Production and consumption of nitric oxide by three methanotrophic bacteria. Appl Environ Microbiol 66: 3891-3897.
94. Yoshinari T, Knowles R, (1976) Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochem Biophys Res Commun 69: 705-710.
95. Braker G, Schwarz J, Conrad R, (2010) Influence of temperature on the composition and activity of denitrifying soil communities. FEMS Microbiol Ecol 73: 134-148.
96. Pieja AJ, Rostkowski KH, Criddle CS, (2011) Distribution and selection of poly-3-hydroxybutyrate production capacity in methanotrophic proteobacteria. Microb Ecol 62: 564-573.
97. Qin L, Liu Y, Tay JH, (2005) Denitrification on poly-beta-hydroxybutyrate in microbial granular sludge sequencing batch reactor. Water Res 39: 1503-1510.
98. Vecherskaya M, Dijkema C, Saad HR, Stams AJM, (2009) Microaerobic and anaerobic metabolism of a Methylocystis parvus strain isolated from a denitrifying bioreactor. Environ Microbiol Rep 1: 442-449.
99. Pieja AJ, Sundstrom ER, Criddle CS, (2011) Poly-3-hydroxybutyrate metabolism in the type II methanotroph Methylocystis parvus OBBP. Appl Environ Microbiol 77: 6012-6019.
100. Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter FJ, et al. (2009) EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10: 154.
101. Strobel T, Al-Dilaimi A, Blom J, Gessner A, Kalinowski J, et al. (2012) Complete genome sequence of Saccharothrix espanaensis DSM 44229T and comparison to the other completely sequenced Pseudonocardiaceae. BMC Genomics 13: 465.
102. Lapidus A, Clum A, LaButti K, Kaluzhnaya MG, Lim S, et al. (2011) Genomes of three methylotrophs from a single niche reveal the genetic and metabolic divergence of the Methylophilaceae. J Bacteriol 193: 3757-3764.
103. Lukjancenko O, Ussery DW, Wassenaar TM, (2012) Comparative genomics of Bifidobacterium, Lactobacillus and related probiotic genera. Microb Ecol 63: 651-673.
104. Shonnard DR, Taylor RT, Tompson A, Knapp RB, (1992) Hydrodynamic effects on microcapillary motility and chemotaxis assays of Methylosinus trichosporium OB3b. Appl Environ Microbiol 58: 2737-2743.
105. Dunfield PF, Yimga MT, Dedysh SN, Berger U, Liesack W, et al. (2002) Isolation of a Methylocystis strain containing a novel pmoA-like gene. FEMS Microbiol Ecol 41: 17-26.
106. Dedysh SN, Belova SE, Bodelier PLE, Smirnova KV, Khmelenina VN, et al. (2007) Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing 'signature' fatty acids of type I methanotrophs. Int J Syst Evol Microbiol 57: 472-479.
107. Bowman JP, Sly LI, Nichols PD, Hayward AC, (1993) Revised taxonomy of the methanotrophs: Description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species, and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Bacteriol 43: 735-753.
108. Wartiainen I, Hestnes AG, McDonald IR, Svenning MM, (2006) Methylocystis rosea sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (78° N). Int J Syst Evol Microbiol 56: 541-547.
109. Lindner AS, Pacheco A, Aldrich HC, Costello Staniec A, Uz I, et al. (2007) Methylocystis hirsuta sp. nov., a novel methanotroph isolated from a groundwater aquifer. Int J Syst Evol Microbiol 57: 1891-1900.
110. Yoon S, Dispirito AA, Kraemer SM, Semrau JD, (2011) A simple assay for screening microorganisms for chalkophore production. Methods Enzymol 495: 247-258.
111. Aziz RK, Breitbart M, Edwards RA, (2010) Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 38: 4207-4217.
112. Heyer J, Galchenko VF, Dunfield PF, (2002) Molecular phylogeny of type II methane-oxidizing bacteria isolated from various environments. Microbiology 148: 2831-2846.
113. Toukdarian AE, Lidstrom ME, (1984) Nitrogen metabolism in a new obligate methanotroph, 'Methylosinus' strain 6. J Gen Microbiol 130: 1827-1837.
114. Ngugi DK, Brune A, (2012) Nitrate reduction, nitrous oxide formation, and anaerobic ammonia oxidation to nitrite in the gut of soil-feeding termites (Cubitermes and Ophiotermes spp.). Environ Microbiol 14: 860-871.
115. Steingruber SM, Friedrich J, Gachter R, Wehrli B, (2001) Measurement of denitrification in sediments with the 15N isotope pairing technique. Appl Environ Microbiol 67: 3771-3778.
116. Edgar RC, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
117. Talavera G, Castresana J, (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564-577.
118. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
119. Parks DH, Beiko RG, (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26: 715-721.