Comparison of 26 Sphingomonad Genomes Reveals Diverse Environmental Adaptations and Biodegradative Capabilities

Applied and Environmental Microbiology

Volumn 79, Issue 12, 2013, Pages 3724-3733

  Aylward, Frank O ^a   McDonald, Bradon R ^a   Adams, Sandra M ^a   Valenzuela, Alejandra ^a   Schmidt, Rebeccah A ^a   Goodwin, Lynne A ^c,d   Woyke, Tanja ^d   Currie, Cameron R ^a   Suen, Garret ^a   Poulsen, Michael ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL CONTAMINANTS; ENVIRONMENTAL ADAPTATION; GENOME SEQUENCES; GLYCOSIDE HYDROLASES; METABOLIC VERSATILITY; NITROAROMATIC COMPOUND; OLIGOTROPHIC ENVIRONMENT; OPEN READING FRAME;

AMINO ACIDS; DNA; ECOLOGY; ENZYMES; GENE TRANSFER; METABOLISM; NUTRIENTS; PLANTS (BOTANY); STRAIN;

GENES;

ADAPTATION; AMINO ACID; BIODEGRADATION; CATABOLISM; COMPARATIVE STUDY; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GENE TRANSFER; GENOME; MICROBIAL COMMUNITY; NUTRIENT CYCLING; OLIGOTROPHIC ENVIRONMENT; PHYLOGENETICS; PLANT COMMUNITY; SPECIES DIVERSITY;

ADAPTATION; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BACTERIAL GENOME; BIOLOGICAL MODEL; BIOREMEDIATION; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA SEQUENCE; ENVIRONMENT; ENZYMOLOGY; GENETICS; ISOPTERA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PUERTO RICO; SOUTH AFRICA; SPHINGOMONADACEAE;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BIODEGRADATION, ENVIRONMENTAL; CLUSTER ANALYSIS; ENVIRONMENT; GENOME, BACTERIAL; ISOPTERA; MODELS, GENETIC; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; PUERTO RICO; SEQUENCE ANALYSIS, DNA; SOUTH AFRICA; SPHINGOMONADACEAE;

ALPHAPROTEOBACTERIA; NOVOSPHINGOBIUM; SPHINGOBIUM; SPHINGOMONAS; SPHINGOMONAS SP.; SPHINGOPYXIS;

EID: 84878555219     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00518-13     Document Type: Article

References (69)

1. Balkwill DL, Fredrickson J, Romine M. 2006. The prokaryotes: a handbook on the biology of bacteria, p 605-629. Springer, Singapore.
2. Ryan MP, Adley CC. 2010. Sphingomonas paucimobilis: a persistent Gram-negative nosocomial infectious organism. J. Hosp. Infect. 75:153- 157.
3. Miller TR, Delcher AL, Salzberg SL, Saunders E, Detter JC, Halden RU. 2010. Genome sequence of the dioxin-mineralizing bacterium Sphingomonas wittichii RW1. J. Bacteriol. 192:6101- 6102.
4. Hu A, He J, Chu KH, Yu CP. 2011. Genome sequence of the 17β-estradiol-utilizing bacterium Sphingomonas strain KC8. J. Bacteriol. 193: 4266-4267.
5. Eguchi M, Ostrowski M, Fegatella F, Bowman J, Nichols D, Nishino T, Cavicchioli R. 2001. Sphingomonas alaskensis strain AFO1, an abundant oligotrophic ultramicrobacterium from the North Pacific. Appl. Environ. Microbiol. 67:4945- 4954.
6. Farias ME, Revale S, Mancini E, Ordonez O, Turjanski A, Cortez N, Vazquez MP. 2011. Genome sequence of Sphingomonas sp. S17, isolated from an alkaline, hyperarsenic, and hypersaline volcano-associated lake at high altitude in the Argentinean Puna. J. Bacteriol. 193:3686 -3687.
7. Coronado E, Roggo C, Johnson DR, van der Meer JR. 2012. Genomewide analysis of salicylate and dibenzofuran metabolism in Sphingomonas wittichii RW1. Front. Microbiol. 3:300.
8. Rentz JA, Alvarez PJ, Schnoor JL. 2008. Benzo(a)pyrene degradation by Sphingomonas yanoikuyae JAR02. Environ. Pollut. 151:669-677.
9. Wittich RM, Wilkes H, Sinnwell V, Francke W, Fortnagel P. 1992. Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl. Environ. Microbiol. 58:1005-1010.
10. Schmidt S, Wittich RM, Erdmann D, Wilkes H, Francke W, Fortnagel P. 1992. Biodegradation of diphenyl ether and its monohalogenated derivatives by Sphingomonas sp. strain SS3. Appl. Environ. Microbiol. 58: 2744-2750.
11. Sugimoto M, Tanabe M, Hataya M, Enokibara S, Duine JA, Kawai F. 2001. The first step in polyethylene glycol degradation by sphingomonads proceeds via a flavoprotein alcohol dehydrogenase containing flavin adenine dinucleotide. J. Bacteriol. 183:6694-6698.
12. Harms H, Wilkes H, Wittich R, Fortnagel P. 1995. Metabolism of hydroxydibenzofurans, methoxydibenzofurans, acetoxydibenzofurans, and nitrodibenzofurans by Sphingomonas sp. strain HH69. Appl. Environ. Microbiol. 61:2499 -2505.
13. Wilkes H, Wittich R, Timmis KN, Fortnagel P, Francke W. 1996. Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by Sphingomonas sp. strain RW1. Appl. Environ. Microbiol. 62:367-371.
14. Stolz A. 2009. Molecular characteristics of xenobiotic-degrading sphingomonads. Appl. Microbiol. Biotechnol. 81:793- 811.
15. Masai E, Katayama Y, Nishikawa S, Fukuda M. 1999. Characterization of Sphingomonas paucimobilis SYK-6 genes involved in degradation of lignin-related compounds. J. Ind. Microbiol. Biotechnol. 23:364 -373.
16. Sutherland IW, Kennedy L. 1996. Polysaccharide lyases from gellanproducing Sphingomonas spp. Microbiology 142(Part 4):867- 872.
17. Hashimoto W, Miyake O, Momma K, Kawai S, Murata K. 2000. Molecular identification of oligoalginate lyase of Sphingomonas sp. strain A1 as one of the enzymes required for complete depolymerization of alginate. J. Bacteriol. 182:4572- 4577.
18. Hsu SC, Lockwood JL. 1975. Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl. Microbiol. 29: 422-426.
19. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376 -380.
20. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119.
21. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P. 2012. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res. 40:D284-D289. doi:10.1093/nar/gkr1060.
22. Eddy SR. 1998. Profile hidden Markov models. Bioinformatics 14:755- 763.
23. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
24. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35:W182-W185. doi:10.1093/nar/gkm321.
25. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV. 2001. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29:22-28.
26. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389 -3402.
27. Akhter S, Aziz RK, Edwards RA. 2012. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res. 40:e126.
28. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. 2008. KEGGfor linking genomes to life and the environment. Nucleic Acids Res. 36:D480-D484. doi:10.1093/nar/gkm882.
29. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37:D233-D238. doi:10.1093/nar/gkn663.
30. Suen G, Scott JJ, Aylward FO, Adams SM, Tringe SG, Pinto-Tomas AA, Foster CE, Pauly M, Weimer PJ, Barry KW, Goodwin LA, Bouffard P, Li L, Osterberger J, Harkins TT, Slater SC, Donohue TJ, Currie CR. 2010. An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet. 6:e1001129. doi:10.1371/journal.pgen.1001129.
31. Katoh K, Toh H. 2010. Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26:1899 -1900.
32. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688 -2690.
33. Konstantinidis KT, Tiedje JM. 2005. Towards a genome-based taxonomy for prokaryotes. J. Bacteriol. 187:6258-6264.
34. Felsenstein J. 1989. PHYLIP-Phylogeny Inference Package (version 3.2). Cladistics 5:164 -166.
35. Letunic I, Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
36. R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
37. Takeuchi M, Hamana K, Hiraishi A. 2001. Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int. J. Syst. Evol. Microbiol. 51:1405-1417.
38. Copley SD, Rokicki J, Turner P, Daligault H, Nolan M, Land M. 2012. The whole genome sequence of Sphingobium chlorophenolicum L-1: insights into the evolution of the pentachlorophenol degradation pathway. Genome Biol. Evol. 4:184 -198.
39. Schwartz E. 2009. Microbial megaplasmids. Springer-Verlag, Berlin, Germany.
40. Basta T, Keck A, Klein J, Stolz A. 2004. Detection and characterization of conjugative degradative plasmids in xenobiotic-degrading Sphingomonas strains. J. Bacteriol. 186:3862-3872.
41. Masai E, Kamimura N, Kasai D, Oguchi A, Ankai A, Fukui S, Takahashi M, Yashiro I, Sasaki H, Harada T, Nakamura S, Katano Y, Narita-Yamada S, Nakazawa H, Hara H, Katayama Y, Fukuda M, Yamazaki S, Fujita N. 2012. Complete genome sequence of Sphingobium sp. strain SYK-6, a degrader of lignin-derived biaryls and monoaryls. J. Bacteriol. 194:534 -535.
42. Slater SC, Goldman BS, Goodner B, Setubal JC, Farrand SK, Nester EW, Burr TJ, Banta L, Dickerman AW, Paulsen I, Otten L, Suen G, Welch R, Almeida NF, Arnold F, Burton OT, Du Z, Ewing A, Godsy E, Heisel S, Houmiel KL, Jhaveri J, Lu J, Miller NM, Norton S, Chen Q, Phoolcharoen W, Ohlin V, Ondrusek D, Pride N, Stricklin SL, Sun J, Wheeler C, Wilson L, Zhu H, Wood DW. 2009. Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J. Bacteriol. 191:2501-2511.
43. Harayama S, Kok M, Neidle EL. 1992. Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 46:565- 601.
44. Kertesz MA. 2000. Riding the sulfur cycle-metabolism of sulfonates and sulfate esters in gram-negative bacteria. FEMS Microbiol. Rev. 24:135- 175.
45. Klappenbach JA, Dunbar JM, Schmidt TM. 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66:1328 -1333.
46. Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, DeMaere MZ, Ting L, Ertan H, Johnson J, Ferriera S, Lapidus A, Anderson I, Kyrpides N, Munk AC, Detter C, Han CS, Brown MV, Robb FT, Kjelleberg S, Cavicchioli R. 2009. The genomic basis of trophic strategy in marine bacteria. Proc. Natl. Acad. Sci. U. S. A. 106:15527- 15533.
47. Williams TJ, Ertan H, Ting L, Cavicchioli R. 2009. Carbon and nitrogen substrate utilization in the marine bacterium Sphingopyxis alaskensis strain RB2256. ISME J. 3:1036 -1052.
48. Fegatella F, Lim J, Kjelleberg S, Cavicchioli R. 1998. Implications of rRNA operon copy number and ribosome content in the marine oligotrophic ultramicrobacterium Sphingomonas sp. strain RB2256. Appl. Environ. Microbiol. 64:4433- 4438.
49. Nagata Y, Natsui S, Endo R, Ohtsubo Y, Ichikawa N, Ankai A, Oguchi A, Fukui S, Fujita N, Tsuda M. 2011. Genomic organization and genomic structural rearrangements of Sphingobium japonicum UT26, an archetypal gamma-hexachlorocyclohexane-degrading bacterium. Enzyme Microb. Technol. 49:499 -508.
50. Fredrickson JK, Balkwill DL, Romine MF, Shi T. 1999. Ecology, physiology, and phylogeny of deep subsurface Sphingomonas sp. J. Ind. Microbiol. Biotechnol. 23:273-283.
51. Cavicchioli R, Ostrowski M, Fegatella F, Goodchild A, Guixa-Boixereu N. 2003. Life under nutrient limitation in oligotrophic marine environments: an eco/physiological perspective of Sphingopyxis alaskensis (formerly Sphingomonas alaskensis). Microb. Ecol. 45:203-217.
52. Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappe MS, Short JM, Carrington JC, Mathur EJ. 2005. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242-1245.
53. Hubber A, Vergunst AC, Sullivan JT, Hooykaas PJ, Ronson CW. 2004. Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol. Microbiol. 54:561-574.
54. Wenzel M, Schonig I, Berchtold M, Kampfer P, Konig H. 2002. Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J. Appl. Microbiol. 92:32- 40.
55. Balkwill DL, Drake GR, Reeves RH, Fredrickson JK, White DC, Ringelberg DB, Chandler DP, Romine MF, Kennedy DW, Spadoni CM. 1997. Taxonomic study of aromatic-degrading bacteria from deep-terrestrialsubsurface sediments and description of Sphingomonas aromaticivorans sp. nov., Sphingomonas subterranea sp. nov., and Sphingomonas stygia sp. nov. Int. J. Syst. Bacteriol. 47:191-201.
56. Strabala TJ, Macdonald L, Liu V, Smit AM. 2012. Draft genome sequence of Novosphingobium nitrogenifigens Y88T. J. Bacteriol. 194:201.
57. Luo YR, Kang SG, Kim SJ, Kim MR, Li N, Lee JH, Kwon KK. 2012. Genome sequence of benzo(a) pyrene-degrading bacterium Novosphingobium pentaromativorans US6-1. J. Bacteriol. 194:907.
58. Brown SD, Utturkar SM, Klingeman DM, Johnson CM, Martin SL, Land ML, Lu TY, Schadt CW, Doktycz MJ, Pelletier DA. 2012. Twenty-one genome sequences from Pseudomonas species and 19 genome sequences from diverse bacteria isolated from the rhizosphere and endosphere of Populus deltoides. J. Bacteriol. 194:5991-5993.
59. D'Argenio V, Petrillo M, Cantiello P, Naso B, Cozzuto L, Notomista E, Paolella G, Di Donato A, Salvatore F. 2011. De novo sequencing and assembly of the whole genome of Novosphingobium sp. strain PP1Y. J. Bacteriol. 193:4296.
60. Gan HM, Chew TH, Hudson AO, Savka MA. 2012. Genome sequence of Novosphingobium sp. strain Rr 2-17, a nopaline crown gall-associated bacterium isolated from Vitis vinifera L. grapevine. J. Bacteriol. 194:5137- 5138.
61. Anand S, Sangwan N, Lata P, Kaur J, Dua A, Singh AK, Verma M, Kaur J, Khurana JP, Khurana P, Mathur S, Lal R. 2012. Genome sequence of Sphingobium indicum B90A, a hexachlorocyclohexane-degrading bacterium. J. Bacteriol. 194:4471- 4472.
62. Gai Z, Wang X, Tang H, Tai C, Tao F, Wu G, Xu P. 2011. Genome sequence of Sphingobium yanoikuyae XLDN2-5, an efficient carbazoledegrading strain. J. Bacteriol. 193:6404-6405.
63. Shin SC, Kim SJ, Ahn do H, Lee JK, Park H. 2012. Draft genome sequence of Sphingomonas echinoides ATCC 14820. J. Bacteriol. 194: 1843.
64. Gai Z, Wang X, Zhang X, Su F, Wang X, Tang H, Tai C, Tao F, Ma C, Xu P. 2011. Genome sequence of Sphingomonas elodea ATCC 31461, a highly productive industrial strain of gellan gum. J. Bacteriol. 193:7015- 7016.
65. Wang X, Tao F, Gai Z, Tang H, Xu P. 2012. Genome sequence of the welan gum-producing strain Sphingomonas sp. ATCC 31555. J. Bacteriol. 194:5989 -5990.
66. Shin SC, Ahn do H, Lee JK, Kim SJ, Hong SG, Kim EH, Park H. 2012. Genome sequence of Sphingomonas sp. strain PAMC 26605, isolated from arctic lichen (Ochrolechia sp.). J. Bacteriol. 194:1607.
67. Lee J, Shin SC, Kim SJ, Kim BK, Hong SG, Kim EH, Park H, Lee H. 2012. Draft genome sequence of a Sphingomonas sp., an endosymbiotic bacterium isolated from an arctic lichen Umbilicaria sp. J. Bacteriol. 194: 3010-3011.
68. Lee H, Shin SC, Lee J, Kim SJ, Kim BK, Hong SG, Kim EH, Park H. 2012. Genome sequence of Sphingomonas sp. strain PAMC 26621, an arctic-lichen-associated bacterium isolated from a Cetraria sp. J. Bacteriol. 194:3030.
69. Ma Z, Shen X, Hu H, Wang W, Peng H, Xu P, Zhang X. 2012. Genome sequence of Sphingomonas wittichii DP58, the first reported phenazine-1-carboxylic acid-degrading strain. J. Bacteriol. 194:3535-3536.