Exo-metabolome of Pseudovibrio sp. FO-BEG1 analyzed by ultra-high resolution mass spectrometry and the effect of phosphate limitation

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Romano, Stefano ^a   Dittmar, Thorsten ^b   Bondarev, Vladimir ^a   Weber, Ralf J M ^c   Viant, Mark R ^c   Schulz Vogt, Heide N ^d  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b UNIVERSITY OF OLDENBURG   (Germany)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d LEIBNIZ INSTITUTE FOR BALTIC SEA RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DISSOLVED ORGANIC MATTER; PHENOL; PHOSPHATE; POLYPHENOL; ORGANIC COMPOUND;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOCHEMICAL COMPOSITION; CONCENTRATION (PARAMETERS); ELECTROSPRAY MASS SPECTROMETRY; FOURIER TRANSFORM MASS SPECTROMETRY; HETEROTROPHY; MASS SPECTROMETRY; METABOLITE; METABOLOME; NONHUMAN; NUTRIENT DYNAMICS; NUTRIENT LIMITATION; PSEUDOVIBRIO; RECYCLING; SPECIES DIVERSITY; DOSE RESPONSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOMICS; RHODOBACTERACEAE;

DOSE-RESPONSE RELATIONSHIP, DRUG; MASS SPECTROMETRY; METABOLOMICS; ORGANIC CHEMICALS; PHOSPHATES; RHODOBACTERACEAE;

EID: 84900433783     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096038     Document Type: Article

References (80)

1. Carlson CA (2002) Production and removal processes. In: Hansell DA, Carlson CA, editors. Biogeochemistry of marinine Dissolved Organic Matter. San Diego: CA: Elsevier. pp. 91-152.
2. Kujawinski EB (2011) The impact of microbial metabolism on marine dissolved organic matter. Ann Rev Mar Sci 3: 567-599.
3. Oliver SG, Winson MK, Kell DB, Baganz F (1998) Systematic functional analysis of the yeast genome. Trends Biotechnol 16: 373-378. (Pubitemid 28410425)
4. Allen J, Davey HM, Broadhurst D, Heald JK, Rowland JJ, et al. (2003) High-throughput classification of yeast mutants for functional genomics using metabolic footprinting. Nat Biotechnol 21: 692-696. (Pubitemid 36638098)
5. Fiehn O (2001) Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comp Funct Genomics 2: 155-168.
6. Mapelli V, Olsson L, Nielsen J (2008) Metabolic footprinting in microbiology: methods and applications in functional genomics and biotechnology. Trends Biotechnol 26: 490-497.
7. Cundy KV, Willard KE, Valeri LJ, Shanholtzer CJ, Singh J, et al. (1991) Comparison of traditional Gas-Chromatography (Gc), headspace Gc, and the microbial identification library Gc system for the identification of Clostridium difficile. J Clin Microbiol 29: 260-263.
8. Shnayderman M, Mansfield B, Yip P, Clark HA, Krebs MD, et al. (2005) Species-specific bacteria identification using differential mobility spectrometry and bioinformatics pattern recognition. Anal Chem 77: 5930-5937. (Pubitemid 41324293)
9. Carlier JP (1990) Identification by quantitative gas-chromatography of common Fusobacterium species isolated from clinical specimens. Lett Appl Microbiol 11: 133-136.
10. Brauer MJ, Yuan J, Bennett BD, Lu WY, Kimball E, et al. (2006) Conservation of the metabolomic response to starvation across two divergent microbes. Proc Natl Acad Sci U S A 103: 19302-19307. (Pubitemid 46026027)
11. Coucheney E, Daniell TJ, Chenu C, Nunan N (2008) Gas chromatographic metabolic profiling: a sensitive tool for functional microbial ecology. J Microbiol Methods 75: 491-500.
12. Boersma MG, Solyanikova IP, Van Berkel WJH, Vervoort J, Golovleva LA, et al. (2001) F-19 NMR metabolomics for the elucidation of microbial degradation pathways of fluorophenols. J Ind Microbiol Biotechnol 26: 22-34. (Pubitemid 32568452)
13. Rinas U, Hellmuth K, Kang RJ, Seeger A, Schlieker H (1995) Entry of Escherichia coli into stationary phase is indicated by endogenous and exogenous accumulation of nucleobases. Appl Environ Microbiol 61: 4147-4151.
14. Want EJ, Nordstrom A, Morita H, Siuzdak G (2007) From exogenous to endogenous: The inevitable imprint of mass spectrometry in metabolomics. J Proteome Res 6: 459-468. (Pubitemid 46340150)
15. Junot C, Madalinski G, Tabet JC, Ezan E (2010) Fourier transform mass spectrometry for metabolome analysis. Analyst 135: 2203-2219.
16. Aharoni A, Ric de Vos CH, Verhoeven HA, Maliepaard CA, Kruppa G, et al. (2002) Nontargeted metabolome analysis by use of Fourier transform ion cyclotron mass spectrometry. Omics 6: 217-234. (Pubitemid 35278415)
17. Brown SC, Kruppa G, Dasseux JL (2005) Metabolomics applications of FT-ICR mass spectrometry. Mass Spectrom Rev 24: 223-231. (Pubitemid 40328975)
18. Marshall AG (2004) Accurate mass measurement: taking full advantage of nature's isotopic complexity. Physica B-Condensed Matter 346: 503-508.
19. Rosselló-Móra R, Lucio M, Peña A, Brito-Echeverria J, López-López A, et al. (2008) Metabolic evidence for biogeographic isolation of the extremophilic bacterium Salinibacter ruber. ISME J 2: 242-253. (Pubitemid 351334273)
20. Brito-Echeverria J, Lucio M, López-López A, Antón J, Schmitt-Kopplin P, et al. (2011) Response to adverse conditions in two strains of the extremely halophilic species Salinibacter ruber. Extremophiles 15: 379-389.
21. Takahashi H, Kai K, Shinbo Y, Tanaka K, Ohta D, et al. (2008) Metabolomics approach for determining growth-specific metabolites based on Fourier transform ion cyclotron resonance mass spectrometry. Anal Bioanal Chem 391: 2769-2782.
22. Antón J, Lucio M, Peña A, Cifuentes A, Brito-Echeverria J, et al. (2013) High metabolomic microdiversity within co-occurring Isolates of the extremely halophilic bacterium Salinibacter ruber. PLoS ONE 8(5): e64701. doi:64710.61371/journal.pone.0064701.
23. Bondarev V, Richter M, Romano S, Piel J, Schwedt A, et al. (2013) The genus Pseudovibrio contains metabolically versatile bacteria adapted for symbiosis. Environ Microbiol 15: 2095-2113.
24. Enticknap JJ, Kelly M, Peraud O, Hill RT (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72: 3724-3732. (Pubitemid 43728031)
25. O' Halloran JA, Barbosa TM, Morrissey JP, Kennedy J, O' Gara F, et al. (2011) Diversity and antimicrobial activity of Pseudovibrio spp. from Irish marine sponges. J Appl Microbiol 110: 1495-1508.
26. Flemer B, Kennedy J, Margassery LM, Morrissey JP, O'Gara F, et al. (2012) Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia sp. J Appl Microbiol 112: 289-301.
27. Kennedy J, Baker P, Piper C, Cotter PD, Walsh M, et al. (2009) Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar Biotechnol (NY) 11: 384-396.
28. Thingstad TF, Krom MD, Mantoura RFC, Flaten GAF, Groom S, et al. (2005) Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309: 1068-1071. (Pubitemid 41134463)
29. Cotner JB, Ammerman JW, Peele ER, Bentzen E (1997) Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13: 141-149. (Pubitemid 127472851)
30. Wu JF, Sunda W, Boyle EA, Karl DM (2000) Phosphate depletion in the western North Atlantic Ocean. Science 289: 759-762. (Pubitemid 30650192)
31. Martín JF (2004) Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 186: 5197-5201.
32. Martín JF, Sola-Landa A, Santos-Beneit F, Fernández- Martínez LT, Prieto C, et al. (2011) Cross-talk of global nutritional regulators in the control of primary and secondary metabolism in Streptomyces. Microb Biotechnol 4: 165-174.
33. Shieh WY, Lin YT, Jean WD (2004) Pseudovibrio denitrificans gen. nov., sp. nov., a marine, facultatively anaerobic, fermentative bacterium capable of denitrification. Int J Syst Evol Microbiol 54: 2307-2312. (Pubitemid 39585423)
34. Dittmar T, Koch B, Hertkorn N, Kattner G (2008) A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater. Limnol Oceanogr Methods 6: 230-235. (Pubitemid 351949834)
35. Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 4-9. http://palaeo-electronica.org/2001-1/past/issue1-01.htm
36. Koch BP, Dittmar T (2006) From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter. Rapid Commun Mass Spectrom 20: 926-932. (Pubitemid 43326704)
37. Šantl-Temkiv T, Finster K, Dittmar T, Hansen BM, Thyrhaug R, et al. (2013) Hailstones: a window into the microbial and chemical inventory of a storm cloud. PLoS ONE 8(1): e53550. doi:53510.51371/journal.pone.0053550.
38. Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, et al. (2007) Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3: 211-221. (Pubitemid 47470690)
39. Weber RJM, Viant MR (2010) MI-Pack: increased confidence of metabolite identification in mass spectra by integrating accurate masses and metabolic pathways. Chemometr Intell Lab Syst 104: 75-82.
40. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30. (Pubitemid 30047706)
41. Wishart DS, Knox C, Guo AC, Eisner R, Young N, et al. (2009) HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res 37: D603-610.
42. Wishart DS, Knox C, Guo AC, Cheng D, Shrivastava S, et al. (2008) DrugBank: a knowledgebase for drugs, drug actions and drug targets. Nucleic Acids Res 36: D901-906. (Pubitemid 351149842)
43. Dictionary of Natural Products (2014) Chapman & Hall/CRC Informa, London Version 22.2.
44. Bruhn JB, Nielsen KF, Hjelm M, Hansen M, Bresciani J, et al. (2005) Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter clade. Appl Environ Microbiol 71: 7263-7270. (Pubitemid 43194220)
45. Benning C, Huang ZH, Gage DA (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch Biochem Biophys 317: 103-111.
46. Minnikin DE, Baddiley J, Abdolrah.H (1972) Variation of polar lipid composition of Bacillus subtilis (Marburg) with different growth conditions. FEBS Lett 27: 16-18.
47. Robertson BR, Button DK (1979) Phosphate-limited continuous culture of Rhodotorula rubra - Kinetics of transport, leakage, and growth. J Bacteriol 138: 884-895. (Pubitemid 9209687)
48. Ogawa H, Amagai Y, Koike I, Kaiser K, Benner R (2001) Production of refractory dissolved organic matter by bacteria. Science 292: 917-920. (Pubitemid 32422486)
49. Kawasaki N, Benner R (2006) Bacterial release of dissolved organic matter during cell growth and decline: Molecular origin and composition. Limnol Oceanogr 51: 2170-2180. (Pubitemid 44520913)
50. Gruber DF, Simjouw JP, Seitzinger SP, Taghon GL (2006) Dynamics and characterization of refractory dissolved organic matter produced by a pure bacterial culture in an experimental predator-prey system. Appl Environ Microbiol 72: 4184-4191. (Pubitemid 43894885)
51. Barreto MC, Frisvad JC, Larsen TO, Mogensen J, San-Romão MV (2011) Exo-metabolome of some fungal isolates growing on cork-based medium. Eur Food Res Technol 232: 575-582.
52. Maranón E, Cermeno P, Fernández E, Rodríguez J, Zabala L (2004) Significance and mechanisms of photosynthetic production of dissolved organic carbon in a coastal eutrophic ecosystem. Limnol Oceanogr 49: 1652-1666. (Pubitemid 39333104)
53. Nagata T (2000) Production mechanisms of dissolved organic matter; Kirchman DL, editor New York.Wiley-Liss 121-152.
54. Teira E, Pazo MJ, Serret P, Fernandez E (2001) Dissolved organic carbon production by microbial populations in the Atlantic Ocean. Limnol Oceanogr 46: 1370-1377. (Pubitemid 32826519)
55. Penesyan A, Tebben J, Lee M, Thomas T, Kjelleberg S, et al. (2011) Identification of the antibacterial compound produced by the marine epiphytic bacterium Pseudovibrio sp. D323 and related sponge-associated bacteria. Mar Drugs 9: 1391-1402.
56. Roué M, Quévrain E, Domart-Coulon I, Bourguet-Kondracki ML (2012) Assessing calcareous sponges and their associated bacteria for the discovery of new bioactive natural products. Nat Prod Rep 29: 739-751.
57. Scalbert A, Johnson IT, Saltmarsh M (2005) Polyphenols: antioxidants and beyond. Am J Clin Nutr 81: 215s-217s.
58. Yuan ZC, Zaheer R, Finan TM (2005) Phosphate limitation induces catalase expression in Sinorhizobium meliloti, Pseudomonas aeruginosa and Agrobacterium tumefaciens. Mol Microbiol 58: 877-894. (Pubitemid 41532482)
59. Gerard F, Dri AM, Moreau PL (1999) Role of Escherichia coli RpoS, LexA and HNS global regulators in metabolism and survival under aerobic, phosphatestarvation conditions. Microbiology 145: 1547-1562. (Pubitemid 29351999)
60. Moreau PL (2004) Diversion of the metabolic flux from pyruvate dehydrogenase to pyruvate oxidase decreases oxidative stress during glucose metabolism in nongrowing Escherichia coli cells incubated under aerobic, phosphate starvation conditions. J Bacteriol 186: 7364-7368.
61. Seyedsayamdost MR, Carr G, Kolter R, Clardy J (2011) Roseobacticides: small molecule modulators of an algal-bacterial symbiosis. J Am Chem Soc 133: 18343-18349.
62. Thiel V, Brinkhoff T, Dickschat JS, Wickel S, Grunenberg J, et al. (2010) Identification and biosynthesis of tropone derivatives and sulfur volatiles produced by bacteria of the marine Roseobacter clade. Org Biomol Chem 8: 234-246.
63. Greer EM, Aebisher D, Greer A, Bentley R (2008) Computational studies of the tropone natural products, thiotropocin, tropodithietic acid, and troposulfenin. Significance of thiocarbonyl-enol tautomerism. J Org Chem 73: 280-283.
64. Kintaka K, Ono H, Tsubotani S, Harada S, Okazaki H (1984) Thiotropocin, a new sulfur-containing 7-membered-ring antibiotic produced by a Pseudomonas sp. J Antibiot (Tokyo) 37: 1294-1300. (Pubitemid 15220686)
65. Liang L (2003) Investigation of secondary metabolites of North Sea bacteria: fermentation, isolation, structure elucidation and bioactivity. University of Göttingen.136
66. Degrassi G, Aguilar C, Bosco M, Zahariev S, Pongor S, et al. (2002) Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing bacterial sensors. Curr Microbiol 45: 250-254. (Pubitemid 36935591)
67. Holden MT, Ram Chhabra S, de Nys R, Stead P, Bainton NJ, et al. (1999) Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33: 1254-1266. (Pubitemid 29433630)
68. Huang R, Zhou X, Xu T, Yang X, Liu Y (2010) Diketopiperazines from marine organisms. Chem Biodivers 7: 2809-2829.
69. Prasad C (1995) Bioactive cyclic dipeptides. Peptides 16: 151-164.
70. Paczia N, Nilgen A, Lehmann T, Gätgens J, Wiechert W, et al. (2012) Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms. Microb Cell Fact 11: 122.
71. Behrends V, Ebbels TMD, Williams HD, Bundy JG (2009) Time-resolved metabolic footprinting for nonlinear modeling of bacterial substrate utilization. Appl Environ Microbiol 75: 2453-2463.
72. Kramer R (1994) Secretion of amino-acids by bacteria - Physiology and mechanism. FEMS Microbiol Rev 13: 75-93.
73. Herrmann KM (1995) The shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol 107: 7-12.
74. Coble PG (1996) Characterization of marine and terrestrial DOM in seawater using excitation emission matrix spectroscopy. Mar Chem 51: 325-346.
75. Yamashita Y, Tanoue E (2003) Distribution and alteration of amino acids in bulk DOM along a transect from bay to oceanic waters. Mar Chem 82: 145-160. (Pubitemid 37029439)
76. Hosoya S, Yokota A (2007) Pseudovibrio japonicus sp nov., isolated from coastal seawater in Japan. Int J Syst Evol Microbiol 57: 1952-1955. (Pubitemid 47497126)
77. Rossel PE, Vähätalo AV, Witt M, Dittmar T (2013) Molecular composition of dissolved organic matter from a wetland plant (Juncus effusus) after photochemical and microbial decomposition (1.25 yr): Common features with deep sea dissolved organic matter. Org Geochem 60: 62-71.
78. Kujawinski EB, Longnecker K, Blough NV, Del Vecchio R, Finlay L, et al. (2009) Identification of possible source markers in marine dissolved organic matter using ultrahigh resolution mass spectrometry. Geochim Cosmochim Acta 73: 4384-4399.
79. Kind T, Fiehn O (2006) Metabolomic database annotations via query of elemental compositions: mass accuracy is insufficient even at less than 1 ppm. BMC bioinformatics 7: 234.
80. Traxler MF, Kolter R (2012) A massively spectacular view of the chemical lives of microbes. Proc Natl Acad Sci U S A 109: 10128-10129.