How Geobacteraceae may dominate subsurface biodegradation: Physiology of Geobacter metallireducens in slow-growth habitat-simulating retentostats

Environmental Microbiology

Volumn 11, Issue 9, 2009, Pages 2425-2433

  Lin, Bin ^a   Westerhoff, Hans V ^a,b   Röling, Wilfred F M ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b NGI Ecogenomics Consortium   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAQUINONE 2,6 DISULFONATE; ANTHRAQUINONE DERIVATIVE; ANTHRAQUINONE-2,6-DISULFONATE;

ARTICLE; BIOMASS; BIOREACTOR; BIOREMEDIATION; GENE EXPRESSION; GEOBACTER; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; SOIL POLLUTANT;

ANTHRAQUINONES; BIODEGRADATION, ENVIRONMENTAL; BIOMASS; BIOREACTORS; GENE EXPRESSION; GEOBACTER; SOIL POLLUTANTS;

BACTERIA (MICROORGANISMS); GEOBACTER; GEOBACTER METALLIREDUCENS; GEOBACTER SP.; GEOBACTERACEAE;

EID: 69949110616     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.01971.x     Document Type: Article

References (42)

1. Arbige, M. Chesbro, W.R. (1982) Very low growth of Bacillus polymyxa: stringent response and maintenance energy. Arch Microbiol 132 : 338 344.
2. Bencharit, S. Ward, M.J. (2005) Chemotactic responses to metals and anaerobic electron acceptors in Shewanella oneidensis MR-1. J Bacteriol 187 : 5049 5053.
3. Botton, S., van Harmelen, M., Braster, M., Parsons, J.R. Röling, W.F.M. (2007) Dominance of Geobacteraceae. BTX-degrading enrichments from an iron-reducing aquifer. FEMS Microbiol Ecol 62 : 118 130.
4. van Breukelen, B.M., Röling, W.F.M., Groen, J., Griffioen, J. van Verseveld, H.W. (2003) Biogeochemistry and isotope geochemistry of a landfill leachate plume. J Contam Hydrol 65 : 245 268.
5. Bulthuis, B.A., Koningstein, G.M., Stouthamer, A.H. van Verseveld, H.W. (1989) A comparison between aerobic growth of Bacillus licheniformis in continuous culture and partial-recycling fermentor, with contributions to the discussion on maintenance energy demand. Arch Microbiol 152 : 499 507.
6. Champine, J.E., Underhill, B., Johnston, J.M., Lilly, W.W. Goodwin, S. (2000) Electron transfer in the dissimilatory iron-reducing bacterium Geobacter metallireducens. Anaerobe 6 : 187 196.
7. Childers, S.E., Ciufo, S. Lovley, D.R. (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416 : 767 769.
8. Chin, K.J., Esteve-Nunez, A., Leang, C. Lovley, D.R. (2004) Direct correlation between rates of anaerobic respiration and levels of mRNA for key respiratory genes in Geobacter sulfurreducens. Appl Environ Microbiol 70 : 5183 5189.
9. Clark, W.M. (1960) Oxidation-Reduction Potentials of Organic Systems. Baltimore, MD, USA : The Williams & Wilkins Company.
10. Coates, J.D., Phillips, E.J.P., Lonergan, D.J., Jenter, H. Lovley, D.R. (1996) Isolation of Geobacter species from diverse sedimentary environments. Appl Environ Microbiol 62 : 1531 1536.
11. Cummings, D.E., Snoeyenbos-West, O.L., Newby, D.T., Niggemyer, A.M., Lovley, D.R., Achenbach, L.A. Rosenzweig, R.F. (2003) Diversity of Geobacteraceae species inhabiting metal-polluted freshwater lake sediments ascertained by 16S rDNA analyses. Microb Ecol 46 : 257 269.
12. Esteve-Nunez, A., Rothermich, M., Sharma, M. Loveley, D.R. (2005) Growth of Geobacter sulfurreducens under nutrient-limiting conditions in continuous culture. Environ Microbiol 7 : 641 649.
13. Finneran, K.T., Housewright, M.E. Lovley, D.R. (2002) Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol 4 : 510 516.
14. Holmes, D.E., Finneran, K.T., O'Neil, R.A. Lovley, D.R. (2002) Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium- contaminated aquifer sediments. Appl Environ Microbiol 68 : 2300 2306.
15. Holmes, D.E., Nevin, K.P. Lovley, D.R. (2004a) In situ expression of nifD in Geobacteraceae in subsurface sediments. Appl Environ Microbiol 70 : 7251 7259.
16. Holmes, D.E., Nevin, K.P. Lovley, D.R. (2004b) Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov. Int J Syst Evol Microbiol 54 : 1591 1599.
17. Hua, Q., Yang, C., Oshima, T., Mori, H. Shimizu, K. (2004) Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Appl Environ Microbiol 70 : 2354 2366.
18. Islam, F.S., Gault, A.G., Boothman, C., Polya, D.A., Charnock, J.M., Chatterjee, D. Lloyd, J.R. (2004) Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430 : 68 71.
19. Lin, B., Braster, M., Röling, W.F.M. van Breukelen, B.M. (2007) Iron-reducing microorganisms in a landfill leachate-polluted aquifer: complementing culture-independent information with enrichments and isolations. Geomicrobiol J 24 : 283 294.
20. Lovley, D.R. Phillips, E.J.P. (1988) Novel mode of microbial energy-metabolism - organic-carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54 : 1472 1480.
21. Lovley, D.R., Giovannoni, S.J., White, D.C., Champine, J.E., Phillips, E.J.P., Gorby, Y.A. Goodwin, S. (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159 : 336 344.
22. Lovley, D.R., Coates, J.D., Blunt-Harris, E.L., Phillips, E.J.P. Woodward, J.C. (1996) Humic substances as electron acceptors for microbial respiration. Nature 382 : 445 448.
23. Lovley, D.R., Fraga, J.L., Blunt-Harris, E.L., Hayes, L.A., Phillips, E.J.P. Coates, J.D. (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim Hydrobiol 26 : 152 157.
24. Lovley, D.R., Holmes, D.E. Nevin, K.P. (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49 : 219 286.
25. Mailloux, B.J. Fuller, M.E. (2003) Determination of in situ bacterial growth rates in aquifers and aquifer sediments. Appl Environ Microbiol 69 : 3798 3808.
26. Müller, R.H. Babel, W. (1996) Measurement of growth at very low rates (mu >= 0), an approach to study the energy requirement for the survival of Alcaligenes eutrophus JMP 134. Appl Environ Microbiol 62 : 147 151.
27. Neal, A.L., Rosso, K.M., Geesey, G.G., Gorby, Y.A. Little, B.J. (2003) Surface structure effects on direct reduction of iron oxides by Shewanella oneidensis. Geochim Cosmochim Acta 67 : 4489 4503.
28. O'Neil, R.A., Holmes, D.E., Coppi, M.V., Adams, L.A., Larrahondo, M.J., Ward, J.E., et al. (2008) Gene transcript analysis of assimilatory iron limitation in Geobacteraceae during groundwater bioremediation. Environ Microbiol 10 : 1218 1230.
29. Roden, E.E. Zachara, J.M. (1996) Microbial reduction of crystalline iron(III) oxides: influence of oxide surface area and potential for cell growth. Environ Sci Technol 30 : 1618 1628.
30. Röling, W.F.M., van Breukelen, B.M., Braster, M., Lin, B. van Verseveld, H.W. (2001) Relationships between microbial community structure and hydrochemistry in a landfill leachate-polluted aquifer. Appl Environ Microbiol 67 : 4619 4629.
31. Rooney-Varga, J.N., Anderson, R.T., Fraga, J.L., Ringelberg, D. Lovley, D.R. (1999) Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl Environ Microbiol 65 : 3056 3063.
32. Schrickx, J.M., Krave, A.S., Verdoes, J.C., Van den Hondel, C.A.M.J.J., Stouthamer, A.H. Van Verseveld, H.W. (1993) Growth and product formation in chemostat and recycling cultures by Aspergillus niger N402 and a glucoamylase overproducing transformant, provided with multiple copies of the glaA gene. J Gen Microbiol 139 : 2801 2810.
33. Schwertmann, U. Cornell, R.M. (1991) Iron Oxides in the Laboratory: Preparation and Characterization. New York, NY, USA : VCH Publishers.
34. Snoeyenbos-West, O.L., Nevin, K.P., Anderson, R.T. Lovley, D.R. (2000) Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb Ecol 39 : 153 167.
35. Tappe, W., Laverman, A., Bohland, M., Braster, M., Rittershaus, S., Groeneweg, J., et al. (1999) Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention. Appl Environ Microbiol 65 : 2471 2477.
36. Tijhuis, L., Van Loosdrecht, M.C.M. Heijnen, J.J. (1993) A thermodynamically based correlation for maintenance Gibbs energy-requirements in aerobic and anaerobic chemotropic growth. Biotechnol Bioeng 42 : 509 519.
37. Tros, M.E., Bosma, T.N.P., Schraa, G. Zehnder, A.J.B. (1996) Measurement of minimum substrate concentration (S-min) in a recycling fermenter and its prediction from the kinetic parameters of Pseudomonas sp. strain B13 from batch and chemostat cultures. Appl Environ Microbiol 62 : 3655 3661.
38. 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.
39. van Verseveld, H.W., de Hollander, J.A., Frankena, J., Braster, M., Leeuwerik, F.J. Stouthamer, A.H. (1986) Modelling of microbial substrate conversion, growth and product formation in a recycling fermentor. Antonie Van Leeuwenhoek 52 : 325 342.
40. Viollier, E., Inglett, P.W., Hunter, K., Roychoudhury, A.N. Van Cappellen, P. (2000) The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl Geochem 15 : 785 790.
41. Winderl, C., Schaefer, S. Lueders, T. (2007) Detection of anaerobic toluene and hydrocarbon degraders in contaminated aquifers using benzylsuccinate synthase (bssA) genes as a functional marker. Environ Microbiol 9 : 1035 1046.
42. Zehnder, A.J.B. (1989) Biology of Anaerobic Microorganisms. New York, USA : John Wiley and Sons.