Ecophysiology of Thioploca ingrica as revealed by the complete genome sequence supplemented with proteomic evidence

ISME Journal

Volumn 9, Issue 5, 2015, Pages 1166-1176

  Kojima, Hisaya ^a   Ogura, Yoshitoshi ^b   Yamamoto, Nozomi ^c   Togashi, Tomoaki ^c   Mori, Hiroshi ^c   Watanabe, Tomohiro ^a   Nemoto, Fumiko ^a   Kurokawa, Ken ^c   Hayashi, Tetsuya ^b   Fukui, Manabu ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b UNIVERSITY OF MIYAZAKI   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; CHROMOSOME; DNA; ECOPHYSIOLOGY; GENOME; LACUSTRINE DEPOSIT; MICROBIAL ACTIVITY; PROTEOMICS;

BACTERIA (MICROORGANISMS); THIOPLOCA; THIOPLOCA INGRICA;

CARBON; FRESH WATER; NITRIC ACID DERIVATIVE; PROTEOME; SULFUR;

BACTERIAL GENE; BACTERIAL GENOME; CHEMISTRY; DNA SEQUENCE; ECOSYSTEM; GENETICS; JAPAN; LAKE; METABOLISM; METAGENOMICS; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; PROTEOMICS; THIOTRICHACEAE;

CARBON; ECOSYSTEM; FRESH WATER; GENES, BACTERIAL; GENOME, BACTERIAL; JAPAN; LAKES; METAGENOMICS; NITRATES; PHYLOGENY; PROTEOME; PROTEOMICS; SEQUENCE ANALYSIS, DNA; SULFUR; THIOTRICHACEAE; WATER MICROBIOLOGY;

EID: 84928586427     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.209     Document Type: Article

References (54)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, MillerWet al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleid Acids Res 25: 3389-3402
2. Beutler M, Milucka J, Hinck S, Schreiber F, Brock J, Mussmann M et al. (2012). Vacuolar respiration of nitrate coupled to energy conservation in filamentous Beggiatoaceae. Environ Microbiol 14: 2911-2919
3. Brock J, Rhiel E, Beutler M, Salman V, Schulz-Vogt HN. (2012). Unusual polyphosphate inclusions observed in a marine Beggiatoa strain. Antonie Van Leeuwenhoek 101: 347-357
4. Brock J, Schulz-Vogt HN. (2011). Sulfide induces phosphate release from polyphosphate in cultures of a marine Beggiatoa strain. ISME J 5: 497-506
5. Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R. (2013). Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process. Microbiology 159: 2626-2638
6. Dermott R, Legner M. (2002). Dense mat-forming bacterium Thioploca ingrica (Beggiatoaceae) in eastern Lake Ontario: implications to the benthic food web. J Great Lakes Res 28: 688-697
7. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J. (2001). Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?. Appl Environ Microbiol 67: 2873-2882
8. Hensen D, Sperling D, Trü per HG, Brune DC, Dahl C. (2006). Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol Microbiol 62: 794-810
9. Høgslund S, Nielsen JL, Nielsen LP. (2010). Distribution, ecology and molecular identification of Thioploca from Danish brackish water sediments. FEMS Microbiol Ecol 73: 110-120
10. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J et al. (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265-1272
11. Jewell T, Huston SL, Nelson DC. (2008). Methylotrophy in freshwater Beggiatoa alba strains. Appl Environ Microbiol 74: 5575-5578
12. Kajitani R, Toshimoto K, Noguchi H, Toyoda A, Ogura Y, Okuno M et al. (2014). Efficient De novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res 24: 1384-1395
13. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. (2014). Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42: D199-D205
14. Kappler U, Bailey S. (2005). Molecular basis of intramolecular electron transfer in sulfite-oxidizing enzymes is revealed by high resolution structure of a heterodimeric complex of the catalytic molybdopterin subunit and a c-Type cytochrome subunit. J Biol Chem 280: 24999-25007
15. Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG et al. (2000). Sulfite: Cytochrome c oxidoreductase from Thiobacillus novellus. Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J Biol Chem 275: 13202-13212
16. Kappler U, Maher MJ. (2013). The bacterial SoxAX cytochromes. Cell Mol Life Sci 70: 977-992
17. Katoh K, Standley DM. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772-780
18. Kojima H, Koizumi Y, Fukui M. (2006). Community structure of bacteria associated with sheaths of freshwater and brackish Thioploca species. Microb Ecol 52: 765-773
19. Kojima H, Nakajima T, Fukui M. (2007). Carbon source utilization and accumulation of respiration-related substances by freshwater Thioploca species. FEMS Microbiol Ecol 59: 23-31
20. Kojima H, Teske A, Fukui M. (2003). Morphological and phylogenetic characterizations of freshwater Thioploca species from Lake Biwa, Japan, and Lake Constance, Germany. Appl Environ Microbiol 69: 390-398
21. Lagesen K, Hallin PF, Rødland E, Stærfeldt HH, Rognes T, Ussery DW. (2007). RNammer: consistent annotation of rRNA genes in genomic sequences. Nucleic Acids Res 35: 3100-3108
22. Lauterborn R. (1907). Eine neue Gattung Der Schwefelbakterien (Thioploca schmidlei nov. gen. nov. spec.). Ber Dtsch Bot Ges 25: 238-242
23. Lenk S, Moraru C, Hahnke S, Arnds J, Richter M, Kube M et al. (2012). Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J 6: 2178-2187
24. Li H, Durbin R. (2009). Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25: 1754-1760
25. Li L, Stoeckert CJ Jr, Roos DS. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189
26. Lowe TM, Eddy SR. (1997). tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964
27. Lucht JM, Bremer E. (1994). Adaptation of Escherichia coli to high osmolarity environments: osmoregulation of the high-Affinity glycine betaine transport system ProU. FEMS Microbiol Rev 14: 3-20
28. MacGregor BJ, Biddle JF, Harbort C, Matthysse AG, Teske A. (2013a). Sulfide oxidation, nitrate respiration, carbon acquisition, and electron transport pathways suggested by the draft genome of a single orange Guaymas Basin Beggiatoa (Cand. Maribeggiatoa) sp. filament Mar Genomics 11: 53-55
29. MacGregor BJ, Biddle JF, Teske A. (2013b). Mobile elements in a single-filament orange Guaymas Basin Beggiatoa sp. genome: evidence for genetic exchange with cyanobacteria. Appl Environ Microbiol 79: 3974-3985
30. Maier SH, Murray GE. (1965). The fine structure of Thioploca ingrica and a comparison with Beggiatoa. Can J Microbiol 11: 645-663
31. Maier S. (1984). Description of Thioploca ingrica sp. nov., nom. rev. Int J Syst Bacteriol 34: 344-345
32. McHatton SC, Barry JP, Jannasch HW, Nelson DC. (1996). High nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp. Appl Environ Microbiol 62: 954-958
33. McKay LJ, MacGregor BJ, Biddle JF, Albert DB, Mendlovitz HP, Hoer DR et al. (2012). Spatial heterogeneity and underlying geochemistry of phylogenetically diverse orange and white Beggiatoa mats in Guaymas Basin hydrothermal sediments. Deep-Sea Res I 67: 21-31
34. Mu-mann M, Hu FZ, Richter M, De Beer D, Preisler A, Jørgensen BB et al. (2007). Insightsinto the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biol 5: 1923-1937
35. Nelson DC, Waterbury John B, Jannasch Holger W. (1982). Nitrogen fixation and nitrate utilization by marine and freshwater Beggiatoa. Arch Microbiol 133: 172-177
36. Nemoto F, Kojima H, Fukui M. (2011). Diversity of freshwater Thioploca species and their specific association with filamentous bacteria of the phylum Chloroflexi. Microb Ecol 62: 753-764
37. Nemoto F, Kojima H, Ohtaka A, Fukui M. (2012). Filamentous sulfur-oxidizing bacteria of the genus Thioploca from Lake Tonle Sap in Cambodia. Aquat Microb Ecol 66: 295-300
38. Nishino M, Fukui M, Nakajima T. (1998). Dense mats of Thioploca, gliding filamentous sulfur-oxidizing bacteria in Lake Biwa, central Japan. Water Res 32: 953-957
39. Noguchi H, Taniguchi T, Itoh T. (2008). MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res 15: 387-396
40. Pott A.S. Dahl C. 1998. Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur Microbiology 144 1881-1894
41. Prokopenko M.G. Hirst M.B. De Brabandere L. Lawrence D.J. Berelson W.M. Granger J. et al. 2013 Nitrogen losses in anoxicmarine sediments driven by Thioploca-Anammox bacterial consortia Nature 500 194-198
42. Raes J, Korbel JO, Lercher MJ, von Mering C, Bork P. (2007). Prediction of effective genome size in metagenomic samples. Genome Biol 8: R10
43. Salman V, Amann R, Girnth AC, Polerecky L, Bailey JV, Høgslund S et al. (2011). A single-cell sequencing approach to the classification of large, vacuolated sulfur bacteria. System Appl Microbiol 34: 243-259
44. Salman V, Bailey JV, Teske A. (2013). Phylogenetic and morphologic complexity of giant sulphur bacteria. Antonie Van Leeuwenhoek 104: 169-186
45. Schulz HN, Schulz HD. (2005). Large sulfur bacteria and the formation of phosphorite. Science 307: 416-418
46. Sleator RD, Colin H. (2001). Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26: 49-71
47. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739
48. Watanabe T, Kojima H, Fukui M. (2012). Draft genome sequence of a psychrotolerant sulfur-oxidizing bacterium, Sulfuricella denitrificans skB26, and proteomic insights into cold adaptation. Appl Environ Microbiol 78: 6545-6549
49. Whelan S, Goldman N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691-699
50. Winkel M, De Beer D, Lavik G, Peplies J, Mu-mann M. (2013). Close association of active nitrifiers with Beggiatoa mats covering deep-sea hydrothermal sediments. Environ Microbiol 16: 1612-1626
51. Wislouch SM. (1912). Thioploca ingrica nov. sp. Ber Deutsch Bot Ges 30: 470-474
52. Zemskaya TI, Namsaraev BB, Dul'tseva NM, Khanaeva TA, Golobokova LP, Dubinina GA et a.l. 2001. Ecophysiological characteristics of the mat-forming bacterium Thioploca in bottom sediments of the Frolikha Bay, northern Baikal. Microbiology 70: 335-341
53. Zemskaya TI, Chernitsyna SM, Dul'tseva NM, Sergeeva VN, Pogodaeva TV, Namsaraev BB. (2009). Colorless sulfur bacteria Thioploca from different sites in Lake Baikal. Microbiology 78: 117-124
54. Zopfi J, Kjær T, Nielsen LP, Jørgensen BB. 2001). Ecology of Thioploca spp.: nitrate and sulfur storage in relation to chemical microgradients and influence of Thioploca spp. on the sedimentary nitrogen cycle. Appl Environ Microbiol 67: 5530-5537