Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone National Park

Applied and Environmental Microbiology

Volumn 71, Issue 7, 2005, Pages 3978-3986

  Van Der Meer, Marcel T J ^a,b   Schouten, Stefan ^a   Bateson, Mary M ^b   Nübel, Ulrich ^c   Wieland, Andrea ^d   Kühl, Michael ^d   De Leeuw, Jan W ^a   Damsté, Jaap S Sinninghe ^a   Ward, David M ^b  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b MONTANA STATE UNIVERSITY   (United States)

^c ROBERT KOCH INSTITUTE   (Germany)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CARBONATES; HOT SPRINGS; HYDROGEN; ISOTOPES; METABOLISM; METABOLITES; SOLAR RADIATION;

CYANOBACTERIAL METABOLITES; GREEN NONSULFUR-LIKE BACTERIA (GNSLB); HOT SPRING MICROBIAL MATS; PHOTOHETEROTROPHIC;

BACTERIA;

ACETIC ACID C 13; BICARBONATE C 13; BICARBONATE C 14; CARBON 13; CARBON 14; GLYCOLIC ACID; HYDROGEN; INFUSORIAL EARTH; SULFIDE; UNCLASSIFIED DRUG;

CARBON; CYANOBACTERIUM; DIEL VARIATION; METABOLISM; THERMAL SPRING;

ARTICLE; BACTERIUM; CARBON METABOLISM; CARBON SOURCE; CHLOROFLEXUS; CONTROLLED STUDY; GREEN NONSULFUR LIKE BACTERIA; HETEROTROPHY; LIGHT; LIPID ANALYSIS; MICROBIAL MAT; NATIONAL PARK; NONHUMAN; PERIODICITY; ROSEIFLEXUS; THERMAL SPRING;

CARBON; CARBON ISOTOPES; CARBON RADIOISOTOPES; CHLOROFLEXI; HOT SPRINGS; HYDROGEN SULFIDE; HYDROGEN-ION CONCENTRATION; LIGHT; LIPID METABOLISM; SYNECHOCOCCUS;

NORTH AMERICA; UNITED STATES; WESTERN HEMISPHERE; WORLD; YELLOWSTONE NATIONAL PARK;

CHLOROFLEXUS; CYANOBACTERIA; ROSEIFLEXUS;

EID: 22144448928     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.7.3978-3986.2005     Document Type: Article

References (55)

1. Anderson, K. L., T. A. Tayne, and D. M. Ward. 1987. Formation and fate of fermentation products in hot spring cyanobacterial mats. Appl. Environ. Microbiol. 53:2343-2352.
2. 2 recycling. Int. J. Biol. Macromol. 25:37-42.
3. Bateson, M. M., and D. M. Ward. 1988. Photoexcretion and fate of glycolate in a hot spring cyanobacterial mat. Appl. Environ. Microbiol. 54:1738-1743.
4. Bauld, J., and T. D. Brock. 1973. Ecological studies of Chloroflexis, a gliding photosynthetic bacterium. Arch. Microbiol. 92:267-284.
5. Boomer, S. M., D. P. Lodge, B. E. Dutton, and B. K. Pierson. 2002. Molecular characterization of novel red green nonsulfur bacteria from five distinct hot spring communities in Yellowstone National Park. Appl. Environ. Microbiol. 68:346-355.
6. 13C-labelling of biomarkers. Nature 392:801-805.
7. Castenholz, R. W. 1973. The possible photosynthetic use of sulfide by the filamentous phototrophic bacteria of hot springs. Limnol. Oceanogr. 18:863-876.
8. Ebert, A., and A. Brune. 1997. Hydrogen concentration profiles at the oxicanoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl. Environ. Microbiol. 63:4039-4046.
9. Ferris, M. J., M. Kühl, A. Wieland, and D. M. Ward. 2003. Cyanobacterial ecotypes in different optical microenvironments of a 68°C hot spring mat community revealed by 16S-23S rRNA internal transcribed spacer region variation. Appl. Environ. Microbiol. 69:2893-2898.
10. Ferris, M. J., T. S. Magnuson, J. A. Fagg, R. Thar, M. Kühl, K. B. Sheehan, and J. M. Henson. 2003. Microbially mediated sulphide production in a thermal, acidic algal mat community in Yellowstone National Park. Environ. Microbiol. 5:954-960.
11. Ferris, M. J., S. C. Nold, N. P. Revsbech, and D. M. Ward. 1997. Population structure and physiological changes within a hot spring microbial mat community following disturbance. Appl. Environ. Microbiol. 63:1367-1374.
12. Ferris, M. J., and D. M. Ward. 1997. Seasonal distribution of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 63:1375-1381.
13. Giovannoni, S. J., N. P. Revsbech, D. M. Ward, and R. W. Castenholz. 1987. Obligately phototrophic Chloroflexus: primary production in anaerobic hot spring microbial mats. Arch. Microbiol. 147:80-87.
14. Glud, R. N., N. B. Ramsing, and N. P. Revsbech. 1992. Photosynthesis and photosynthesis-coupled respiration in natural biofilms quantified with oxygen microsensors. J. Phycol. 28:51-60.
15. Grasshoff, K., M. Ehrhardt, and K. Kremling. 1983. Methods of seawater analysis. Verlag Chemie, Weinheim, Germany.
16. Habicht, K. S., A. Wieland, R. N. Glud, and M. Kühl. 2003. Sulfur cycling and sulfur isotope fractionation in a hyperthermal microbial mat of Yellow-stone N.P., p. 61. Aquatic Sciences Meeting of the American Society of Limnology and Oceanography, Salt Lake City, Utah, 8 to 14 February 2003.
17. Kanada, S., S. Takaichi, K. Matsuura, and K. Nakamura. 2002. Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int. J. Syst. Evol. Microbiol. 52:187-193.
18. 13C-NMR. Arch. Microbiol. 148:292-297.
19. 2 fixation of Chloroflexus aurantiacus. Arch. Microbiol. 145:173-180.
20. Konopka, A. 1992. Accumulation and utilization of polysaccharide by hotspring phototrophs during a light-dark transition. FEMS Microbiol. Ecol. 102:27-32.
21. Konopka, A., and M. Schnur. 1980. Effects of light intensity on macromolecular synthesis in cyanobacteria. Methods Enzymol. 6:291-301.
22. Kühl, M., R. N. Glud, H. Ploug, and N. B. Ramsing. 1996. Microenvironmental control of photosynthesis and photosynthesis-coupled respiration in an epilithic Cyanobacterial biofilm. J. Phycol. 32:799-812.
23. 2S microsensor for profiling biofilms and sediments: application in an acidic lake sediment. Aquat. Microb. Ecol. 15:201-209.
24. Madigan, M. T., and T. D. Brock. 1975. Photosynthetic sulfide oxidation by Chloroflexus aurantiacus, a filamentous, photosynthetic, gliding bacterium. J. Bacteriol. 122:782-784.
25. 2 fixation in photosynthetically-grown Chloroflexus aurantiacus. FEMS Microbiol. Lett. 1:301-304.
26. Madigan, M. T., S. R. Petersen, and T. D. Brock. 1974. Nutritional studies on Chloroflexus, a filamentous photosynthetic, gliding bacterium. Arch. Microbiol. 100:97-103.
27. Menendez, C., Z. Bauer, H. Huber, N. Gad'on, K. O. Stetter, and G. Fuchs. 1999. Presence of acetyl coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J. Bacteriol. 181:1088-1098.
28. Nold, S. C., and D. M. Ward. 1996. Photosynthate partitioning and fermentation in hot spring microbial mat communities. Appl. Environ. Microbiol. 62:4598-4607.
29. Norman, E. G., and B. Colman. 1992. Formation and metabolism of glycolate in the cyanobacterium Coccochloris peniocystis. Arch. Microbiol. 157:375-380.
30. Nühel, U., M. M. Bateson, V. Vandieken, M. Kühl, and D. M. Ward. 2002. Microscopic examination of distribution and phenotypic properties of phylogenetically diverse Chloroflexaceae-relaited bacteria in hot spring microbial mats. Appl. Environ. Microbiol. 68:4593-4603.
31. Oyaizu, H., B. Debrunner-Vossbrinck, L. Mandelco, J. A. Studier, and C. R. Woese. 1987. The green non-sulfur bacteria: a deep branching in the eubacterial line of descent. Syst. Appl. Microbiol. 9:47-53.
32. Papke, R. T., N. B. Ramsing, M. M. Bateson, and D. M. Ward. 2003. Geographical isolation in hot spring cyanobacteria. Environ. Microbiol. 5:650-659.
33. Pierson, B. K., and R. W. Castenholz. 1974. A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch. Microbiol. 100:5-24.
34. Pierson, B. K., and R. W. Castenholz. 1992. The family Chloroflexaceae, p. 3754-3774. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (ed.), The prokaryotes. Springer-Verlag, New York, N.Y.
35. Ramsing, N. B., M. J. Ferris, and D. M. Ward. 2000. Highly ordered vertical structure of Synechococcus populations within the one-millimeter-thick photic zone of a hot spring cyanobacterial mat. Appl. Environ. Microbiol. 66:1038-1049.
36. Revsbech, N. P. 1989. An oxygen microelectrode with a guard cathode. Limnol. Oceanogr. 34:474-478.
37. Revsbech, N. P., and D. M. Ward. 1984. Microelectrode studies of interstitial water chemistry and photosynthetic activity in a hot spring microbial mat. Appl. Environ. Microbiol. 48:270-275.
38. Revsbech, N. P., and D. M. Ward. 1984. Microprofiles of dissolved substances and photosynthesis in microbial mats measured with microelectrodes, p. 171-188. In Y. Cohen, R. W. Castenholz, and H. O. Halvorson (ed.), Microbial mats: stromatolites. Alan R. Liss, Inc., New York, N.Y.
39. Ruff-Roberts, A. L., J. G. Kuenen, and D. M. Ward. 1994. Distribution of cultivated and uncultivated cyanobacteria and Chloroflexus-like bacteria in hot spring microbial mats. Appl. Environ. Microbiol. 60:697-704.
40. Sakata, S., J. M. Hayes, A. R. McTaggart, R. A. Evans, K. J. Leckrone, and R. K. Togasaki. 1997. Carbon isotopic fractionation associated with lipid biosynthesis by a cyanobacterium: relevance for interpretation of biomarker records. Geochim. Cosmochim. Acta 61:5379-5389.
41. Sandbeck, K. A., and D. M. Ward. 1981. Fate of immediate methane precursors in low sulfate hot spring algal-bacterial mats. Appl. Environ. Microbiol. 41:775-782.
42. Schouten, S., W. C. M. K. Breteler, P. Blokker, N. Schogt, W. I. C. Rijpstra, K. Grice, M. Baas, and J. S. S. Damsté. 1998. Biosynthetic effects on the stable carbon isotopic composition of algal lipids: implications for deciphering the carbon isotopic biomarker record. Geochim. Cosmochim. Acta 62:1397-1406.
43. Schulz, H. N., and B. B. Jørgensen. 2001. Big bacteria. Annu. Rev. Microbiol. 55:105-137.
44. Shiea, J., S. C. Brassell, and D. M. Ward. 1990. Mid-chain branched mono-and dimethyl alkanes in hot spring cyanobacterial mats: a direct biogenic source for branched alkanes in ancient sediments. Org. Geochem. 15:223-231.
45. Shiea, J., S. C. Brassell, and D. M. Ward. 1991. Comparative analysis of extractable lipids in hot spring microbial mats and their component photosynthetic bacteria. Org. Geochem. 17:309-319.
46. van der Meer, M. T. J., S. Schouten, J. W. de Leeuw, and D. M. Ward. 2000. Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopicaliy heavy organic carbon in the geological record. Environ. Microbiol. 2:428-435.
47. van der Meer, M. T. J., S. Schouten, S. Hanada, E. C. Hopmans, J. S. S. Damsté, and D. M. Ward. 2002. Alkane-1,2-diol-based glycosides and fatty glycosides and wax esters in Roseiflexus castenholzii and hot spring microbial mats. Arch. Microbiol. 178:229-237.
48. van der Meer, M. T. J., S. Schouten, J. S. S. Damsté, J. W. de Leeuw, and D. M. Ward. 2003. Compound-specific isotopic fractionation patterns suggest different carbon metabolisms among Chloroflexus-like bacteria in hot spring microbial mats. Appl. Environ. Microbiol. 69:6000-6006.
49. 13C-contents of organic components in the photoautotrophic bacterium Chloroflexus aurantiacus. J. Biol. Chem. 276:10971-10976.
50. Ward, D. M., M. J. Ferris, S. C. Nold, and M. M. Bateson. 1998. A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol. Mol. Biol. Rev. 62:1353-1370.
51. Ward, D. M., C. Santegoeds, S. C. Nold, N. B. Ramsing, M. J. Ferris, and M. M. Bateson. 1997. Biodiversity within hot spring microbial mat communities: molecular monitoring of enrichment cultures. Antonie Leeuwenhoek. 71:143-150.
52. Ward, D. M., T. A. Tayne, K. L. Anderson, and M. M. Bateson. 1987. Community structure and interactions among community members in hot spring cyanobacterial mats, p. 179-210. In M. Fletcher, T. R. G. Gray, and J. G. Jones (ed.), Ecology of microbial communities. Cambridge University Press, Cambridge, United Kingdom.
53. Wieland, A., and M. Kühl. 2000. Short term temperature effects on oxygen and sulfide cycling in a hyper-saline cyanobacterial mat (Solar Lake, Egypt). Marine Ecol. Prog. Ser. 196:87-102.
54. Zeng, Y. B., D. M. Ward, S. C. Brassell, and G. Eglinton. 1992. Biogeochemistry of hot spring environments. 3. Apolar and polar lipids in the biologically active layers of a cyanobacterial mat. Chem. Geol. 95:347-360.
55. Zinder, S. H., W. N. Doemel, and T. D. Brock. 1977. Production of volatile sulfur compounds during the decomposition of algal mats. Appl. Environ. Microbiol. 34:859-860.