1887

Abstract

Aerobic anoxygenic photosynthesis (AAP) is found in an increasing number of proteobacterial strains thriving in ecosystems ranging from extremely oligotrophic to eutrophic. Here, we have investigated whether the fuel oxygenate-degrading betaproteobacterium L108 can use AAP to compensate kinetic limitations at low heterotrophic substrate fluxes. In a fermenter experiment with complete biomass retention and also during chemostat cultivation, strain L108 was challenged with extremely low substrate feeding rates of -butyl alcohol (TBA), an intermediate of methyl -butyl ether (MTBE). Interestingly, formation of photosynthetic pigments, identified as bacteriochlorophyll and spirilloxanthin, was only induced in growing cells at TBA feeding rates less than or equal to maintenance requirements observed under energy excess conditions. Growth continued at rates between 0.001 and 0.002 h even when the TBA feed was decreased to values close to 30 % of this maintenance rate. Partial sequencing of genomic DNA of strain L108 revealed a bacteriochlorophyll synthesis gene cluster () and photosynthesis regulator genes ( and ) typically found in AAP and other photosynthetic proteobacteria. The usage of light as auxiliary energy source enabling evolution of efficient degradation pathways for kinetically limited heterotrophic substrates and for lowering the threshold substrate concentration at which growth becomes zero is discussed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.068957-0
2013-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/10/2180.html?itemId=/content/journal/micro/10.1099/mic.0.068957-0&mimeType=html&fmt=ahah

References

  1. Agalidis I., Mattioli T., Reiss-Husson F.( 1999). Spirilloxanthin is released by detergent from Rubrivivax gelatinosus reaction center as an aggregate with unusual spectral properties. Photosynth Res 62:31–42 [View Article]
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.( 1997). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  3. Berghoff B. A., Glaeser J., Nuss A. M., Zobawa M., Lottspeich F., Klug G.( 2011). Anoxygenic photosynthesis and photooxidative stress: a particular challenge for Roseobacter.. Environ Microbiol 13:775–791 [View Article][PubMed]
    [Google Scholar]
  4. Chance B.( 1952). Spectra and reaction kinetics of respiratory pigments of homogenized and intact cells. Nature 169:215–221 [View Article][PubMed]
    [Google Scholar]
  5. Chesbro W. R., Evans T., Eifert R.( 1979). Very slow growth of Escherichia coli.. J Bacteriol 139:625–638[PubMed]
    [Google Scholar]
  6. Csotonyi J. T., Swiderski J., Stackebrandt E., Yurkov V.( 2010). A new extreme environment for aerobic anoxygenic phototrophs: biological soil crusts. Adv Exp Med Biol 675:3–14 [View Article][PubMed]
    [Google Scholar]
  7. Deeb R. A., Hu H. Y., Hanson J. R., Scow K. M., Alvarez-Cohen L.( 2001). Substrate interactions in BTEX and MTBE mixtures by an MTBE-degrading isolate. Environ Sci Technol 35:312–317 [View Article][PubMed]
    [Google Scholar]
  8. Elsen S., Jaubert M., Pignol D., Giraud E.( 2005). PpsR: a multifaceted regulator of photosynthesis gene expression in purple bacteria. Mol Microbiol 57:17–26 [View Article][PubMed]
    [Google Scholar]
  9. Fuchs B. M., Spring S., Teeling H., Quast C., Wulf J., Schattenhofer M., Yan S., Ferriera S., Johnson J.& other authors ( 2007). Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc Natl Acad Sci U S A 104:2891–2896 [View Article][PubMed]
    [Google Scholar]
  10. Hojerová E., Mašín M., Brunet C., Ferrera I., Gasol J. M., Koblížek M.( 2011). Distribution and growth of aerobic anoxygenic phototrophs in the Mediterranean Sea. Environ Microbiol 13:2717–2725 [View Article][PubMed]
    [Google Scholar]
  11. Hyman M.( 2013). Biodegradation of gasoline ether oxygenates. Curr Opin Biotechnol 24:443–450 [View Article][PubMed]
    [Google Scholar]
  12. Igarashi N., Harada J., Nagashima S., Matsuura K., Shimada K., Nagashima K. V.( 2001). Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria. J Mol Evol 52:333–341[PubMed]
    [Google Scholar]
  13. Imhoff J. F., Trüper H. G.( 1989). Purple nonsulfur bacteria. Bergey's Manual in Systematic Bacteriology1658–1661 Stacey J. T., Bryant M. P., Pfennig N., Holt J. G. Baltimore, Md.: Williams and Wikins;
    [Google Scholar]
  14. Jechalke S., Rosell M., Martínez-Lavanchy P. M., Pérez-Leiva P., Rohwerder T., Vogt C., Richnow H. H.( 2011). Linking low-level stable isotope fractionation to expression of the cytochrome P450 monooxygenase-encoding ethB gene for elucidation of methyl tert-butyl ether biodegradation in aerated treatment pond systems. Appl Environ Microbiol 77:1086–1096 [View Article][PubMed]
    [Google Scholar]
  15. Kolb A., Püttmann W.( 2006). Comparison of MTBE concentrations in groundwater of urban and nonurban areas in Germany. Water Res 40:3551–3558 [View Article][PubMed]
    [Google Scholar]
  16. Kolber Z. S., Plumley F. G., Lang A. S., Beatty J. T., Blankenship R. E., VanDover C. L., Vetriani C., Koblizek M., Rathgeber C., Falkowski P. G.( 2001). Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495 [View Article][PubMed]
    [Google Scholar]
  17. Lechner U., Brodkorb D., Geyer R., Hause G., Härtig C., Auling G., Fayolle-Guichard F., Piveteau P., Müller R. H., Rohwerder T.( 2007). Aquincola tertiaricarbonis gen. nov., sp. nov., a tertiary butyl moiety-degrading bacterium. Int J Syst Evol Microbiol 57:1295–1303 [View Article][PubMed]
    [Google Scholar]
  18. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J.( 1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275[PubMed]
    [Google Scholar]
  19. Masuda S., Berleman J., Hasselbring B. M., Bauer C. E.( 2008). Regulation of aerobic photosystem synthesis in the purple bacterium Rhodospirillum centenum by CrtJ and AerR. Photochem Photobiol Sci 7:1267–1272 [View Article][PubMed]
    [Google Scholar]
  20. Moran M. J., Zogorski J. S., Squillace P. J.( 2005). MTBE and gasoline hydrocarbons in ground water of the United States. Ground Water 43:615–627 [View Article][PubMed]
    [Google Scholar]
  21. Moskvin O. V., Gilles-Gonzalez M. A., Gomelsky M.( 2010). The PpaA/AerR regulators of photosynthesis gene expression from anoxygenic phototrophic proteobacteria contain heme-binding SCHIC domains. J Bacteriol 192:5253–5256 [View Article][PubMed]
    [Google Scholar]
  22. Müller R. H., Babel W.( 1996). Measurement of growth at very low rates (μ ≥ 0), an approach to study the energy requirement for the survival of Alcaligenes eutrophus JMP 134. Appl Environ Microbiol 62:147–151[PubMed]
    [Google Scholar]
  23. Müller R. H., Rohwerder T., Harms H.( 2007). Carbon conversion efficiency and limits of productive bacterial degradation of methyl tert-butyl ether and related compounds. Appl Environ Microbiol 73:1783–1791 [View Article][PubMed]
    [Google Scholar]
  24. Müller R. H., Rohwerder T., Harms H.( 2008). Degradation of fuel oxygenates and their main intermediates by Aquincola tertiaricarbonis L108. Microbiology 154:1414–1421 [View Article][PubMed]
    [Google Scholar]
  25. Müller S., Harms H., Bley T.( 2010). Origin and analysis of microbial population heterogeneity in bioprocesses. Curr Opin Biotechnol 21:100–113 [View Article][PubMed]
    [Google Scholar]
  26. Pirt S. J.( 1982). Maintenance energy: a general model for energy-limited and energy-sufficient growth. Arch Microbiol 133:300–302 [View Article][PubMed]
    [Google Scholar]
  27. Rohwerder T., Breuer U., Benndorf D., Lechner U., Müller R. H.( 2006). The alkyl tert-butyl ether intermediate 2-hydroxyisobutyrate is degraded via a novel cobalamin-dependent mutase pathway. Appl Environ Microbiol 72:4128–4135 [View Article][PubMed]
    [Google Scholar]
  28. Rohwerder T., Harms H., Müller R. H.( 2011). Synthesis of poly-3-hydroxybutyrate reduces maintenance demand in bacteria growing slowly on methyl tert-butyl ether. J Bioremed Biodegrad [View Article]
    [Google Scholar]
  29. Schäfer F., Muzica L., Schuster J., Treuter N., Rosell M., Harms H., Müller R. H., Rohwerder T.( 2011). Formation of alkenes via degradation of tert-alkyl ethers and alcohols by Aquincola tertiaricarbonis L108 and Methylibium spp. Appl Environ Microbiol 77:5981–5987 [View Article][PubMed]
    [Google Scholar]
  30. Schäfer F., Schuster J., Würz B., Härtig C., Harms H., Müller R. H., Rohwerder T.( 2012). Synthesis of short-chain diols and unsaturated alcohols from secondary alcohol substrates by the Rieske nonheme mononuclear iron oxygenase MdpJ. Appl Environ Microbiol 78:6280–6284 [View Article][PubMed]
    [Google Scholar]
  31. Schmidt T. C., Morgenroth E., Schirmer M., Effenberger M., Haderlein S. B.( 2002). Use and occurrence of fuel oxygenates in Europe. Oxygenates in Gasoline: Environmental Aspects58–79 Diaz A. F., Drogos D. L. Washington, DC: ACS;
    [Google Scholar]
  32. Schuster J., Schäfer F., Hübler N., Brandt A., Rosell M., Härtig C., Harms H., Müller R. H., Rohwerder T.( 2012). Bacterial degradation of tert-amyl alcohol proceeds via hemiterpene 2-methyl-3-buten-2-ol by employing the tertiary alcohol desaturase function of the Rieske nonheme mononuclear iron oxygenase MdpJ. J Bacteriol 194:972–981 [View Article][PubMed]
    [Google Scholar]
  33. Schuster J., Purswani J., Breuer U., Pozo C., Harms H., Müller R. H., Rohwerder T.( 2013). Constitutive expression of the cytochrome P450 EthABCD monooxygenase system enables degradation of synthetic dialkyl ethers in Aquincola tertiaricarbonis L108. Appl Environ Microbiol 79:2321–2327 [View Article][PubMed]
    [Google Scholar]
  34. Seeger E. M., Kuschk P., Fazekas H., Grathwohl P., Kaestner M.( 2011). Bioremediation of benzene-, MTBE- and ammonia-contaminated groundwater with pilot-scale constructed wetlands. Environ Pollut 159:3769–3776 [View Article][PubMed]
    [Google Scholar]
  35. Suyama T., Shigematsu T., Takaichi S., Nodasaka Y., Fujikawa S., Hosoya H., Tokiwa Y., Kanagawa T., Hanada S.( 1999). Roseateles depolymerans gen. nov., sp. nov., a new bacteriochlorophyll a-containing obligate aerobe belonging to the β-subclass of the Proteobacteria. Int J Syst Bacteriol 49:449–457 [View Article][PubMed]
    [Google Scholar]
  36. Suyama T., Shigematsu T., Suzuki T., Tokiwa Y., Kanagawa T., Nagashima K. V. P., Hanada S.( 2002). Photosynthetic apparatus in Roseateles depolymerans 61A is transcriptionally induced by carbon limitation. Appl Environ Microbiol 68:1665–1673 [View Article][PubMed]
    [Google Scholar]
  37. Suzuki M. T., Béjà O.( 2007). An elusive marine photosynthetic bacterium is finally unveiled. Proc Natl Acad Sci U S A 104:2561–2562 [View Article][PubMed]
    [Google Scholar]
  38. Tomasch J., Gohl R., Bunk B., Diez M. S., Wagner-Döbler I.( 2011). Transcriptional response of the photoheterotrophic marine bacterium Dinoroseobacter shibae to changing light regimes. ISME J 5:1957–1968 [View Article][PubMed]
    [Google Scholar]
  39. Tros M. E., Bosma T. N., Schraa G., Zehnder A. J.( 1996). Measurement of minimum substrate concentration (Smin) in a recycling fermentor and its prediction from the kinetic parameters of Pseudomonas strain B13 from batch and chemostat cultures. Appl Environ Microbiol 62:3655–3661[PubMed]
    [Google Scholar]
  40. van Verseveld H. W., Chesbro W. R., Braster M., Stouthamer A. H.( 1984). Eubacteria have 3 growth modes keyed to nutrient flow. Consequences for the concept of maintenance and maximal growth yield. Arch Microbiol 137:176–184 [View Article][PubMed]
    [Google Scholar]
  41. van Wezel A., Puijker L., Vink C., Versteegh A., de Voogt P.( 2009). Odour and flavour thresholds of gasoline additives (MTBE, ETBE and TAME) and their occurrence in Dutch drinking water collection areas. Chemosphere 76:672–676 [View Article][PubMed]
    [Google Scholar]
  42. Wang X., Deshusses M. A.( 2007). Biotreatment of groundwater contaminated with MTBE: interaction of common environmental co-contaminants. Biodegradation 18:37–50 [View Article][PubMed]
    [Google Scholar]
  43. Yaneva N., Schuster J., Schäfer F., Lede V., Przybylski D., Paproth T., Harms H., Müller R. H., Rohwerder T.( 2012). Bacterial acyl-CoA mutase specifically catalyzes coenzyme B12-dependent isomerization of 2-hydroxyisobutyryl-CoA and (S)-3-hydroxybutyryl-CoA. J Biol Chem 287:15502–15511 [View Article][PubMed]
    [Google Scholar]
  44. Yurkov V. V., Beatty J. T.( 1998). Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724[PubMed]
    [Google Scholar]
  45. Yurkova N., Rathgeber C., Swiderski J., Stackebrandt E., Beatty J. T., Hall K. J., Yurkov V.( 2002). Diversity, distribution and physiology of the aerobic phototrophic bacteria in the mixolimnion of a meromictic lake. FEMS Microbiol Ecol 40:191–204 [View Article][PubMed]
    [Google Scholar]
  46. Yutin N., Suzuki M. T., Teeling H., Weber M., Venter J. C., Rusch D. B., Béjà O.( 2007). Assessing diversity and biogeography of aerobic anoxygenic phototrophic bacteria in surface waters of the Atlantic and Pacific Oceans using the Global Ocean Sampling expedition metagenomes. Environ Microbiol 9:1464–1475 [View Article][PubMed]
    [Google Scholar]
  47. Zheng Q., Zhang R., Koblížek M., Boldareva E. N., Yurkov V., Yan S., Jiao N.( 2011). Diverse arrangement of photosynthetic gene clusters in aerobic anoxygenic phototrophic bacteria. PLoS ONE 6:e25050 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.068957-0
Loading
/content/journal/micro/10.1099/mic.0.068957-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error