Metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics

mBio

Volumn 4, Issue 2, 2013, Pages

  Mosier, Annika C ^a   Justice, Nicholas B ^a   Bowen, Benjamin P ^b   Baran, Richard ^b   Thomas, Brian C ^a   Northen, Trent R ^b   Banfield, Jillian F ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; CARBON; COPPER; ECTOINE; HYDROXYECTOINE; IRON; ISOTOPE; NITROGEN; PROTON; SULFATE; SULFUR; TAURINE; UNCLASSIFIED DRUG; ZINC; ACID; METAL;

ACIDITY; ADAPTATION; AMINO ACID METABOLISM; ARTICLE; BIOFILM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FUNGAL METABOLISM; ISOTOPE LABELING; LEPTOSPIRILLUM; MASS SPECTROMETRY; METABOLITE; METABOLOMICS; METAGENOMICS; METAL TOLERANCE; MICROBIAL COMMUNITY; MINING; NONHUMAN; OSMOTIC STRESS; PH; PREDICTION; PRIORITY JOURNAL; PROTEOMICS; TAURINE METABOLISM; TRANSCRIPTOMICS; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; DRUG EFFECT; FUNGUS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ACIDS; ADAPTATION, PHYSIOLOGICAL; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; ENVIRONMENTAL MICROBIOLOGY; FUNGI; ISOTOPE LABELING; MASS SPECTROMETRY; METABOLOMICS; METALS;

EID: 84880077929     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00484-12     Document Type: Article

References (63)

1. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37-43.
2. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F. 2002. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. U. S. A. 99:14250-14255.
3. Wasser JS, Lawler RG, Jackson DC. 1996. Nuclear magnetic resonance spectroscopy and its applications in comparative physiology. Physiol. Zool. 69:1-34.
4. Kristal BS, Vigneau-Callahan KE, Matson WR. 1998. Simultaneous analysis of the majority of low-molecular-weight, redox-active compounds from mitochondria. Anal. Biochem. 263:18-25.
5. Trauger SA, Kalisak E, Kalisiak J, Morita H, Weinberg MV, Menon AL, Poole FL, Adams MW, Siuzdak G. 2008. Correlating the transcriptome, proteome, and metabolome in the environmental adaptation of a hyperthermophile. J. Proteome Res. 7:1027-1035.
6. Kol S, Merlo ME, Scheltema RA, de Vries M, Vonk RJ, Kikkert NA, Dijkhuizen L, Breitling R, Takano E. 2010. Metabolomic characterization of the salt stress response in Streptomyces coelicolor. Appl. Environ. Microbiol. 76:2574-2581.
7. Halter D, Goulhen-Chollet F, Gallien S, Casiot C, Hamelin J, Gilard F, Heintz D, Schaeffer C, Carapito C, Van Dorsselaer A, Tcherkez G, Arsène-Ploetze F, Bertin PN. 2012. In situ proteo-metabolomics reveals metabolite secretion by the acid mine drainage bio-indicator, euglena mutabilis. ISME J. 6:1391-1402.
8. Wilmes P, Bowen BP, Thomas BC, Mueller RS, Denef VJ, VerBerkmoes NC, Hettich RL, Northen TR, Banfield JF. 2010. Metabolome-proteome differentiation coupled to microbial divergence. Mbio 1(5):e00246-10. http://dx.doi.org/10.1128/mBio.00246-10.
9. Druschel G, Baker B, Gihring T, Banfield J. 2004. Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem. Trans. 5:13-32.
10. Bond PL, Druschel GK, Banfield JF. 2000. Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl. Environ. Microbiol. 66:4962-4971.
11. Lo I, Denef VJ, Verberkmoes NC, Shah MB, Goltsman D, DiBartolo G, Tyson GW, Allen EE, Ram RJ, Detter JC, Richardson P, Thelen MP, Hettich RL, Banfield JF. 2007. Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446: 537-541.
12. Simmons SL, Dibartolo G, Denef VJ, Goltsman DS, Thelen MP, Banfield JF. 2008. Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol. 6:e177. http://dx.doi.org/10.1371/journal.pbio.0060177.
13. Denef VJ, Kalnejais LH, Mueller RS, Wilmes P, Baker BJ, Thomas BC, VerBerkmoes NC, Hettich RL, Banfield JF. 2010. Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc. Natl. Acad. Sci. U. S. A. 107:2383-2390.
14. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP, Banfield JF. 2009. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10:R85. http://dx.doi.org/10.1186/gb-2009-10-8-r85.
15. Garcia DE, Baidoo EE, Benke PI, Pingitore F, Tang YJ, Villa S, Keasling JD. 2008. Separation and mass spectrometry in microbial metabolomics. Curr. Opin. Microbiol. 11:233-239.
16. Oldiges M, Lütz S, Pflug S, Schroer K, Stein N, Wiendahl C. 2007. Metabolomics: current state and evolving methodologies and tools. Appl. Microbiol. Biotechnol. 76:495-511.
17. Fiehn O. 2001. Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comp. Funct. Genomics 2:155-168.
18. Baran R, Robert M, Suematsu M, Soga T, Tomita M. 2007. Visualization of three-way comparisons of omics data. BMC Bioinformatics 8:72. http://dx.doi.org/10.1186/1471-2105-8-72.
19. Baran R, Bowen BP, Bouskill NJ, Brodie EL, Yannone SM, Northen TR. 2010. Metabolite identification in Synechococcus sp. PCC 7002 using untargeted stable isotope assisted metabolite profiling. Anal. Chem. 82: 9034-9042.
20. Baran R, Bowen BP, Northen TR. 2011. Untargeted metabolic footprinting reveals a surprising breadth of metabolite uptake and release by Synechococcus sp. PCC 7002. Mol. Biosyst. 7:3200-3206.
21. van der Werf MJ, Overkamp KM, Muilwijk B, Coulier L, Hankemeier T. 2007. Microbial metabolomics: toward a platform with full metabolome coverage. Anal. Biochem. 370:17-25.
22. Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, Botstein D, Rabinowitz JD. 2006. Conservation of the metabolomic response to starvation across two divergent microbes. Proc. Natl. Acad. Sci. U. S. A. 103: 19302-19307.
23. Hegeman AD, Schulte CF, Cui Q, Lewis IA, Huttlin EL, Eghbalnia H, Harms AC, Ulrich EL, Markley JL, Sussman MR. 2007. Stable isotope assisted assignment of elemental compositions for metabolomics. Anal. Chem. 79:6912-6921.
24. Rodgers RP, Blumer EN, Hendrickson CL, Marshall AG. 2000. Stable isotope incorporation triples the upper mass limit for determination of elemental composition by accurate mass measurement. J. Am. Soc. Mass Spectrom. 11:835-840.
25. Bowen BP, Fischer CR, Baran R, Banfield JF, Northen T. 2011. Improved genome annotation through untargeted detection of pathwayspecific metabolites. BMC Genomics 12(Suppl 1):S6. http://dx.doi.org/10.1186/1471-2164-12-S3-S6.
26. Dunn WB, Erban A, Weber RJM, Creek DJ, Brown M, Breitling R, Hankemeier T, Goodacre R, Neumann S, Kopka J, Viant MR. 2012. Mass appeal: metabolite identification in mass spectrometry-focused untargeted metabolomics. Metabolomics 8:1-23.
27. Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TWM, Fiehn O, Goodacre R, Griffin JL, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane AN, Lindon JC, Marriott P, Nicholls AW, Reily MD, Thaden JJ, Viant MR. 2007. Proposed minimum reporting standards for chemical analysis. Metabolomics 3:211-221.
28. Fischer CR, Wilmes P, Bowen BP, Northen TR, Banfield JF. 2011. Deuterium-exchange metabolomics identifies N-methyl lyso phosphatidylethanolamines as abundant lipids in acidophilic mixed microbial communities. Metabolomics 8:566-578.
29. Baker BJ, Lutz MA, Dawson SC, Bond PL, Banfield JF. 2004. Metabolically active eukaryotic communities in extremely acidic mine drainage. Appl. Environ. Microbiol. 70:6264-6271.
30. Baker BJ, Tyson GW, Goosherst L, Banfield JF. 2009. Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Appl. Environ. Microbiol. 75:2192-2199.
31. Huxtable RJ. 1992. Physiological actions of taurine. Physiol. Rev. 72: 101-163.
32. Schuller-Levis GB, Park E. 2003. Taurine: new implications for an old amino acid. FEMS Microbiol. Lett. 226:195-202.
33. Stapley EO, Starkey RL. 1970. Decomposition of cysteic acid and taurine by soil micro-organisms. J. Gen. Microbiol. 64:77-84.
34. Denger K, Smits TH, Cook AM. 2006. Genome-enabled analysis of the utilization of taurine as sole source of carbon or of nitrogen by Rhodobacter sphaeroides 2.4.1. Microbiology 152:3197-3206.
35. Cayley S, Lewis BA, Guttman HJ, Record MT. 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo. J. Mol. Biol. 222: 281-300.
36. da Costa MS, Santos H, Galinski EA. 1998. An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv. Biochem. Eng. Biotechnol. 61:117-153.
37. Lentzen G, Schwarz T. 2006. Extremolytes: natural compounds from extremophiles for versatile applications. Appl. Microbiol. Biotechnol. 72: 623-634.
38. Pastor JM, Salvador M, Argandoña M, Bernal V, Reina-Bueno M, Csonka LN, Iborra JL, Vargas C, Nieto JJ, Cánovas M. 2010. Ectoines in cell stress protection: uses and biotechnological production. Biotechnol. Adv. 28:782-801.
39. Fontana M, Duprè S, Pecci L. 2006. The reactivity of hypotaurine and cysteine sulfinic acid with peroxynitrite. Adv. Exp. Med. Biol. 583:15-24.
40. Coloso RM, Hirschberger LL, Dominy JE, Lee J-I, Stipanuk MH. 2006. Cysteamine dioxygenase: evidence for the physiological conversion of cysteamine to hypotaurine in rat and mouse tissues. Adv. Exp. Med. Biol. 583:25-36.
41. Cook AM, Denger K. 2006. Metabolism of taurine in microorganisms: a primer in molecular biodiversity? Adv. Exp. Med. Biol. 583:3-13.
42. Eichhorn E, van der Ploeg JR, Kertesz MA, Leisinger T. 1997. Characterization of alpha-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J. Biol. Chem. 272:23031-23036.
43. van der Ploeg JR, Weiss MA, Saller E, Nashimoto H, Saito N, Kertesz MA, Leisinger T. 1996. Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. J. Bacteriol. 178:5438-5446.
44. Caspi R, Altman T, Dale JM, Dreher K, Fulcher CA, Gilham F, Kaipa P, Karthikeyan AS, Kothari A, Krummenacker M, Latendresse M, Mueller LA, Paley S, Popescu L, Pujar A, Shearer AG, Zhang P, Karp PD. 2010. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 38:D473-D479. http://dx.doi.org/10.1093/nar/gkp875.
45. Louis P, Galinski EA. 1997. Characterization of genes for the biosynthesis of the compatible solute ectoine from Marinococcus halophilus and osmoregulated expression in Escherichia coli. Microbiology 143:1141-1149.
46. Cánovas D, Vargas C, Iglesias-Guerra F, Csonka LN, Rhodes D, Ventosa A, Nieto JJ. 1997. Isolation and characterization of salt-sensitive mutants of the moderate halophile Halomonas elongata and cloning of the ectoine synthesis genes. J. Biol. Chem. 272:25794-25801.
47. García-Estepa R, Argandoña M, Reina-Bueno M, Capote N, Iglesias- Guerra F, Nieto JJ, Vargas C. 2006. The ectD gene, which is involved in the synthesis of the compatible solute hydroxyectoine, is essential for thermoprotection of the halophilic bacterium Chromohalobacter salexigens. J. Bacteriol. 188:3774-3784.
48. Prabhu J, Schauwecker F, Grammel N, Keller U, Bernhard M. 2004. Functional expression of the ectoine hydroxylase gene (thpD) from Streptomyces chrysomallus in Halomonas elongata. Appl. Environ. Microbiol. 70:3130-3132.
49. Lippert K, Galinski EA. 1992. Enzyme stabilization be ectoine-type compatible solutes: protection against heating, freezing and drying. Appl. Microbiol. Biotechnol. 37:61-65.
50. Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PS, Chan PP, Gollabgir A, Hemp J, Hügler M, Karr EA, Könneke M, Shin M, Lawton TJ, Lowe T, Martens- Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. U. S. A. 107:8818-8823.
51. Goltsman DS, Denef VJ, Singer SW, VerBerkmoes NC, Lefsrud M, Mueller RS, Dick GJ, Sun CL, Wheeler KE, Zemla A, Baker BJ, Hauser L, Land M, Shah MB, Thelen MP, Hettich RL, Banfield JF. 2009. Community genomic and proteomic analyses of chemoautotrophic ironoxidizing "Leptospirillum rubarum" (group II) and "Leptospirillum ferrodiazotrophum" (group III) bacteria in acid mine drainage biofilms. Appl. Environ. Microbiol. 75:4599-4615.
52. Belnap CP, Pan C, VerBerkmoes NC, Power ME, Samatova NF, Carver RL, Hettich RL, Banfield JF. 2010. Cultivation and quantitative proteomic analyses of acidophilic microbial communities. ISME J. 4:520-530.
53. Belnap CP, Pan C, Denef VJ, Samatova NF, Hettich RL, Banfield JF. 2011. Quantitative proteomic analyses of the response of acidophilic microbial communities to different pH conditions. ISME J. 5:1152-1161.
54. Mueller RS, Dill BD, Pan C, Belnap CP, Thomas BC, VerBerkmoes NC, Hettich RL, Banfield JF. 2011. Proteome changes in the initial bacterial colonist during ecological succession in an acid mine drainage biofilm community. Environ. Microbiol. 13:2279-2292.
55. Jiao Y, Cody GD, Harding AK, Wilmes P, Schrenk M, Wheeler KE, Banfield JF, Thelen MP. 2010. Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl. Environ. Microbiol. 76:2916-2922.
56. Davey ME, O'Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847-867.
57. Jebbar M, Sohn-Bösser L, Bremer E, Bernard T, Blanco C. 2005. Ectoine-induced proteins in Sinorhizobium meliloti include an ectoine ABC-type transporter involved in osmoprotection and ectoine catabolism. J. Bacteriol. 187:1293-1304.
58. Schwibbert K, Marin-Sanguino A, Bagyan I, Heidrich G, Lentzen G, Seitz H, Rampp M, Schuster SC, Klenk H-P, Pfeiffer F, Oesterhelt D, Kunte HJ. 2011. A blueprint of ectoine metabolism from the genome of the industrial producer Halomonas elongata DSM 2581(T). Environ. Microbiol. 13:1973-1994.
59. Vargas C, Jebbar M, Carrasco R, Blanco C, Calderón MI, Iglesias- Guerra F, Nieto JJ. 2006. Ectoines as compatible solutes and carbon and energy sources for the halophilic bacterium Chromohalobacter salexigens. J. Appl. Microbiol. 100:98-107.
60. Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.
61. Bond PL, Banfield JF. 2001. Design and performance of rRNA targeted oligonucleotide probes for in situ detection and phylogenetic identification of microorganisms inhabiting acid mine drainage environments. Microb. Ecol. 41:149-161.
62. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I. 2012. The genome portal of the department of energy joint genome institute. Nucleic Acids Res. 40:D26-D32. http://dx.doi.org/10.1093/nar/gkr947.
63. 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. http://dx.doi.org/10.1093/nar/gkm321.