Community structure and function of high-temperature chlorophototrophic microbial mats inhabiting diverse geothermal environments

Frontiers in Microbiology

Volumn 4, Issue JUN, 2013, Pages

  Klatt, Christian G ^a   Inskeep, William P ^a   Herrgard, Markus J ^b   Jay, Zackary J ^a   Rusch, Douglas B ^c   Tringe, Susannah G ^d   Parenteau, M Niki ^e,f   Ward, David M ^a   Boomer, Sarah M ^g   Bryant, Donald A ^a,h   Miller, Scott R ⁱ  

^a MONTANA STATE UNIVERSITY   (United States)

^b Chalmers University of Technology   (Denmark)

^c INDIANA UNIVERSITY   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

^e Search for Extraterrestrial Intelligence Institute   (United States)

^f NASA AMES RESEARCH CENTER   (United States)

^g WESTERN OREGON UNIVERSITY   (United States)

^h PENNSYLVANIA STATE UNIVERSITY   (United States)

ⁱ UNIVERSITY OF MONTANA   (United States)

Author keywords

Functional genomics; Microbial interactions; Microbial mats; Phototrophic bacteria; Thermophilic bacteria

Indexed keywords

BACTERIOCHLOROPHYLL; HYDRACRYLIC ACID; IRON; RNA 16S; SULFUR;

ANAEROBIC METABOLISM; ARTICLE; CARBON FIXATION; CHLOROPHOTOTROPHY; DNA EXTRACTION; ECOSYSTEM; FUNCTIONAL GENOMICS; GEOCHEMICAL ANALYSIS; METAGENOME; MICROBIAL MAT; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISMAL INTERACTION; OXIDATION KINETICS; PHOTOTROPHIC BACTERIUM; PHOTOTROPHY; PHYLOGENY; QUANTITATIVE ANALYSIS; RNA SEQUENCE; YELLOWSTONE GEOTHERMAL ECOSYSTEM;

BACTEROIDETES; CHLOROBIALES; CHLOROFLEXI; CHLOROFLEXI (CLASS); CHLOROFLEXUS; CYANOBACTERIA; FIRMICUTES; FISCHERELLA; GAMMAPROTEOBACTERIA; PHOTOBACTERIA; ROSEIFLEXUS; SYNECHOCOCCUS; THERMOCHROMATIUM;

EID: 84884224944     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00106     Document Type: Article

References (105)

1. Anderson, K. L., Tayne, T. A., and Ward, D. M. (1987). Formation and fate of fermentation products in hot spring cyanobacterial mats. Appl. Environ. Microbiol. 53, 2343-2352.
2. Badger, J. H., Hoover, T. R., Brun, Y. V., Weiner, R. M., Laub, M. T., Alexandre, G., et al. (2006). Comparative genomic evidence for a close relationship between the dimorphic prosthecate bacteria Hyphomonas neptunium and Caulobacter crescentus. J. Bacteriol. 188, 6841-6850.
3. Becraft, E. D., Cohan, F. M., Kuhl, M., Jensen, S. I., and Ward, D. M. (2011). Fine-scale distribution patterns of Synechococcus ecological diversity in microbial mats of Mushroom Spring, Yellowstone National Park. Appl. Environ. Microbiol. 77, 7689-7697.
4. Bhaya, D., Grossman, A. R., Steunou, A.-S., Khuri, N., Cohan, F. M., Hamamura, N., et al. (2007). Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J. 1, 703-713.
5. Boomer, S. M., Lodge, D. P., Dutton, B. E., and Pierson, B. (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. Boomer, S. M., Pierson, B. K., Austinhirst, R., and Castenholz, R. W. (2000). Characterization of novel bacteriochlorophyll-a-containing red filaments from alkaline hot springs in Yellowstone National Park. Arch. Microbiol. 174, 152-161.
7. Boyd, E. S., Fecteau, K. M., and Peters, J. W. (2012). Modeling the habitat range of phototrophs in Yellowstone National Park: toward the development of a comprehensive fitness landscape. Front. Microbiol. 3:221. doi:10.3389/fmicb.2012.00221
8. Brock, T. D. (1967). Life at high temperatures. Science 158, 1012-1019.
9. Brock, T. D. (1973). Lower pH limit for the existence of blue-green algae: evolutionary and ecological implications. Science 179, 480-483.
10. Brock, T. D. (1978). Thermophilic Microorganisms and Life at High Temperatures. New York: Springer Verlag.
11. Bryant, D. A., Costas, A. M. G., Maresca, J. A., Chew, A. G. M., Klatt, C. G., Bateson, M. M., et al. (2007). Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317, 523-526.
12. Bryant, D. A., Klatt, C. G., Frigaard, N.-U., Liu, Z., Li, T., Zhao, F., et al. (2012). "Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria," in Functional Genomics and Evolution of Photosynthetic Systems, Vol. 33, Advances in Photosynthesis and Respiration, eds R. L. Burnap, and W. Vermaas (Dordrecht: Springer), 47-102.
13. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., et al. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi:10.1186/1471-2105-10-421
14. Castenholz, R. W. (1969). Thermophilic blue-green algae and the thermal environment. Bacteriol. Rev. 33, 476-504.
15. Castenholz, R. W. (1976). The effect of sulfide on the blue-green algae of hot springs. I. New Zealand and Iceland. J. Phycol. 12, 54-68.
16. Castenholz, R. W. (1977). The effect of sulfide on the blue-green algae of hot springs II. Yellowstone National Park. Microb. Ecol. 3, 79-105.
17. Castenholz, R. W., and Pierson, B. K. (1995). "Ecology of thermophilic anoxygenic phototrophs," in Anoxygenic Photosynthetic Bacteria, eds R. E. Blankenship, M. T. Madigan, and C. E. Bauer (Dordrecht: Kluwer Academic Publishers), 87-103.
18. Chan, L.-K., Morgan-Kiss, R. M., and Hanson, T. E. (2009). Functional analysis of three sulfide:quinone oxidoreductase homologs in Chlorobaculum tepidum. J. Bacteriol. 191, 1026-1034.
19. Cohen, Y., and Rosenberg, E. (eds) (1989). Microbial Mats: Physiological Ecology of Benthic Microbial Communities. Washington, DC: American Society for Microbiology.
20. Colwell, R. K. (2009). EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 8.0. Available at: http://viceroy.eeb.uconn.edu/estimates
21. Cox, A., Shock, E. L., and Havig, J. R. (2011). The transition to microbial photosynthesis in hot spring ecosystems. Chem. Geol. 280, 344-351.
22. Croal, L. R., Jiao, Y., and Newman, D. K. (2007). The fox operon from Rhodobacter strain SW2 promotes phototrophic Fe(II) oxidation in Rhodobacter capsulatus SB1003. J. Bacteriol. 189, 1774-1782.
23. Dahl, C., Engels, S., Pott-Sperling, A. S., Schulte, A., Sander, J., Lübbe, Y., et al. (2005). Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J. Bacteriol. 187, 1392-1404.
24. Eddy, S. R. (2011). Accelerated profile HMM searches. PLoS Comput. Biol. 7:e1002195. doi:10.1371/journal.pcbi.1002195
25. Frigaard, N., and Dahl, C. (2009). Sulfur metabolism in phototrophic sulfur bacteria. Adv. Microb. Physiol. 54, 103-200.
26. Garcia Costas, A. M., Liu, Z., Tomsho, L. P., Schuster, S. C., Ward, D. M., and Bryant, D. A. (2012). Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. Environ. Microbiol. 14, 177-190.
27. Gascuel, O. (1997). BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 14, 685-695.
28. Giovannoni, S., Revsbech, N. P., Ward, D. M., and Castenholz, R. W. (1987). Obligately phototrophic Chloroflexus: primary production in anaerobic hot spring microbial mats. Arch. Microbiol. 147, 80-87.
29. Gotelli, N. J., and Entsminger, G. L. (2001). EcoSim: Null Models Software for Ecology. Version 7.0. Acquired Intelligence Inc. and Kesey-Bear. Available at: http://garyentsminger.com/ecosim/index.htm
30. Gower, J. C. (1971). A general coefficient of similarity and some of its properties. Biometrics 27, 857-871.
31. Gregersen, L. H., Bryant, D. A., and Frigaard, N.-U. (2011). Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front. Microbiol. 2:116. doi:10.3389/fmicb.2011.00116
32. Griesbeck, C., Schütz, M., Schödl, T., Bathe, S., Nausch, L., Mederer, N., et al. (2002). Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41, 11552-11565.
33. Grimm, F., Franz, B., and Dahl, C. (2011). Regulation of dissimilatory sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum. Front. Microbiol. 2:51. doi:10.3389/fmicb.2011.00051
34. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321.
35. Hanada, S., Takaichi, S., Matsuura, K., and Nakamura, K. (2002). Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int. J. Syst. Evol. Microbiol. 52, 187-193.
36. Heidelberg, J. F., Nelson, W. C., Schoenfeld, T., and Bhaya, D. (2009). Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS ONE 4:e4169. doi:10.1371/journal.pone.0004169
37. Henry, E. A., Devereux, R., Maki, J. S., Gilmour, C. C., Woese, C. R., Mandelco, L., et al. (1994). Characterization of a new thermophilic sulfate-reducing bacterium Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov.: its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the bacterial domain. Arch. Microbiol. 161, 62-69.
38. Hiraishi, A. (1997). Transfer of the bacteriochlorophyll b-containing phototrophic bacteria Rhodopseudomonas viridis and Rhodopseudomonas sulfoviridis to the genus Blastochloris gen. nov. Int. J. Syst. Bacteriol. 47, 217-219.
39. Holo, H., and Sirevåg, R. (1986). Autotrophic growth and CO2 fixation of Chloroflexus aurantiacus. Arch. Microbiol. 145, 173-180.
40. Huang, X., and Madan, A. (1999). CAP3: a DNA sequence assembly program. Genome Res. 9, 868-877.
41. Huber, T., Faulkner, G., and Hugenholtz, P. (2004). Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20, 2317-2319.
42. Huson, D. H., Auch, A. F., Qi, J., and Schuster, S. C. (2007). MEGAN analysis of metagenomic data. Genome Res. 17, 377-386.
43. Inskeep, W. P., Ackerman, G. G., Taylor, W. P., Kozubal, M., Korf, S., and Macur, R. E. (2005). On the energetics of chemolithotrophy in nonequilibrium systems: case studies of geothermal springs in Yellowstone National Park. Geobiology 3, 297-317.
44. Inskeep, W. P., Jay, Z. J., Tringe, S. G., Herrgard, M. J., Rusch, D. B., et al. (2013). The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front. Microbiol. 4:67. doi:10.3389/fmicb.2013.00067
45. Inskeep, W. P., Rusch, D. B., Jay, Z. J., Herrgard, M. J., Kozubal, M. A., Richardson, T. H., et al. (2010). Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS ONE 5:e9773. doi:10.1371/journal.pone.0009773
46. Jackson, T. J., Ramaley, R. F., and Meinschein, W. G. (1973). Thermomicrobium, a new genus of extremely thermophilic bacteria. Int. J. Syst. Bacteriol. 23, 28-36.
47. Jensen, S. I., Steunou, A.-S., Bhaya, D., Kuhl, M., and Grossman, A. R. (2011). In situ dynamics of O2, pH and cyanobacterial transcripts associated with CCM, photosynthesis and detoxification of ROS. ISME J. 5, 317-328.
48. Jiao, Y., and Newman, D. K. (2007). The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765-1773.
49. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
50. Klatt, C. G., Bryant, D. A., and Ward, D. M. (2007). Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. Environ. Microbiol. 9, 2067-2078.
51. Klatt, C. G., Liu, Z., Ludwig, M., Kühl, M., Jensen, S. I., Bryant, D. A., et al. (2013). Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring. ISME J. doi:10.1038/ismej.2013.52
52. Klatt, C. G., Wood, J. M., Rusch, D. B., Bateson, M. M., Hamamura, N., Heidelberg, J. F., et al. (2011). Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J. 5, 1262-1278.
53. Liu, Z., Klatt, C. G., Ludwig, M., Rusch, D. B., Jensen, S. I., Kühl, M., et al. (2012). 'Candidatus Thermochlorobacter aerophilum:' an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME J. 6, 1869-1882.
54. Liu, Z., Klatt, C. G., Wood, J. M., Rusch, D. B., Ludwig, M., Wittekindt, N., et al. (2011). Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J. 5, 1279-1290.
55. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371.
56. Macur, R. E., Langner, H. W., Kocar, B. D., and Inskeep, W. P. (2004). Linking geochemical processes with microbial community analysis: successional dynamics in an arsenic-rich, acid-sulfate-chloride geothermal spring. Geobiology 2, 163-177.
57. Madigan, M. T. (1984). A novel photosynthetic purple bacterium isolated from a Yellowstone hot spring. Science 225, 313-315.
58. Madigan, M. T., and Brock, T. D. (1975). Photosynthetic sulfide oxidation by Chloroflexus aurantiacus, a filamentous, photosynthetic, gliding bacterium. J. Bacteriol. 122, 782-784.
59. Madigan, M. T., Jung, D. O., Karr, E. A., Sattley, W. M., Achenbach, L. A., and van der Meer, M. T. J. (2005). "Diversity of anoxygenic phototrophs in contrasting extreme environments," in Geothermal Biology and Geochemsistry in Yellowstone National Park, eds W. P. Inskeep, and T. R. McDermott (Bozeman: Montana State University Publications), 203-219.
60. Madigan, M. T., Petersen, S. R., and Brock, T. D. (1974). Nutritional studies on Chloroflexus, a filamentous photosynthetic, gliding bacterium. Arch. Microbiol. 100, 97-103.
61. Madigan, M. T., Takigiku, R., Lee, R. G., Gest, H., and Hayes, J. M. (1989). Carbon isotope fractionation by thermophilic phototrophic sulfur bacteria: evidence for autotrophic growth in natural populations. Appl. Environ. Microbiol. 55, 639-644.
62. Marcia, M., Ermler, U., Peng, G., and Michel, H. (2009). The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc. Natl. Acad. Sci. U.S.A. 106, 9625-9630.
63. Markowitz, V. M., Chen, I.-M. A., Chu, K., Szeto, E., Palaniappan, K., Grechkin, Y., et al. (2012). IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res. 40, D123-D129.
64. Mavromatis, K., Ivanova, N., Chen, A., Szeto, E., Markowitz, V., and Kyrpides, N. C. (2009). Standard operating procedure for the annotations of microbial genomes by the production genomic facility of the DOE JGI. Stand. Genomic Sci. 1, 63-67.
65. McClesky, R. B., Ball, J. A., Nordstrom, D. K., Holloway, J. M., and Taylor, H. E. (2005). Water-chemistry Data for Selected Hot Springs, Geysers, and Streams in Yellowstone National Park, Wyoming, 2001-2002. Open-File Report 2004-1316. Reston, VA: U.S. Geological Survey.
66. Melendrez, M. C., Lange, R. K., Cohan, F. M., and Ward, D. M. (2011). Influence of molecular resolution on sequence-based discovery of ecological diversity among Synechococcus populations in an alkaline siliceous hot spring microbial mat. Appl. Environ. Microbiol. 77, 1359-1367.
67. Miller, J. R., Delcher, A. L., Koren, S., Venter, E., Walenz, B. P., Brownley, A., et al. (2008). Aggressive assembly of pyrosequencing reads with mates. Bioinformatics 24, 2818-2824.
68. Miller, S. R., Castenholz, R. W., and Pedersen, D. (2007). Phylogeography of the thermophilic cyanobacterium Mastigocladus laminosus. Appl. Environ. Microbiol. 73, 4751-4759.
69. Miller, S. R., Purugganan, M. D., and Curtis, S. E. (2006). Molecular population genetics and phenotypic diversification of two populations of the thermophilic cyanobacterium Mastigocladus laminosus. Appl. Environ. Microbiol. 72, 2793-2800.
70. Miller, S. R., Strong, A. L., Jones, K. L., and Ungerer, M. C. (2009). Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl. Environ. Microbiol. 75, 4565-4572.
71. Nold, S. C., and Ward, D. M. (1996). Photosynthate partitioning and fermentation in hot spring microbial mat communities. Appl. Environ. Microbiol. 62, 4598-4607.
72. Nübel, U., Bateson, M. M., Vandieken, V., Wieland, A., Kuhl, M., and Ward, D. M. (2002). Microscopic examination of distribution and phenotypic properties of phylogenetically diverse Chloroflexaceae-related bacteria in hot spring microbial mats. Appl. Environ. Microbiol. 68, 4593-4603.
73. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., and Etalname, A. (2012). Vegan: Community Ecology Package. R Package Version 2.0-5. Available at: http://CRAN.R-project.org/package=vegan
74. Parks, D. H., and Beiko, R. G. (2010). Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26, 715-721.
75. Pfennig, N. (1974). Rhodopseudomonas globiformis, sp. n., a new species of the Rhodospirillaceae. Arch. Microbiol. 100, 197-206.
76. Pierson, B. K., and Castenholz, R. W. (1974). A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch. Microbiol. 100, 5-24.
77. Pierson, B. K., Parenteau, M. N., and Griffin, B. M. (1999). Phototrophs in high-iron-concentration microbial mats: physiological ecology of phototrophs in an iron-depositing hot spring. Appl. Environ. Microbiol. 65, 5474-5483.
78. R Development Core Team. (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at: URL http://www.R-project.org
79. Rappé, M. S., and Giovannoni, S. J. (2003). The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369-394.
80. Rowe, J. J., Fournier, R. O., and Morey, G. W. (1973). Chemical Analysis of Thermal Waters in Yellowstone National Park, Wyoming, 1960-65. USGS Open File Report. Available at: http://pubs.er.usgs.gov/
81. Rusch, D. B., Halpern, A. L., Sutton, G., Heidelberg, K. B., Williamson, S., Yooseph, S., et al. (2007). The sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5:e77. doi:10.1371/journal.pbio.0050077
82. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., et al. (2003). TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374-378.
83. Selengut, J. D., Haft, D. H., Davidsen, T., Ganapathy, A., Gwinn-Giglio, M., Nelson, W. C., et al. (2007). TIGRFAMs and genome properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res. 35, D260-D264.
84. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.
85. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
86. Strauss, G., and Fuchs, G. (1993). Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur. J. Biochem. 215, 633-643.
87. Taffs, R., Aston, J. E., Brileya, K., Jay, Z., Klatt, C. G., McGlynn, S., et al. (2009). In silico approaches to study mass and energy flows in microbial consortia: a syntrophic case study. BMC Syst. Biol. 3:114. doi:10.1186/1752-0509-3-114
88. Tang, K.-H., Barry, K., Chertkov, O., Dalin, E., Han, C., Hauser, L., et al. (2011). Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics 12:334. doi:10.1186/1471-2164-12-334
89. Teeling, H., Meyerdierks, A., Bauer, M., Amann, R., and Glöckner, F. O. (2004). Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ. Microbiol. 6, 938-947.
90. Trouwborst, R. E., Johnston, A., Koch, G., Luther, G. W. I. I. I., and Pierson, B. K. (2007). Biogeochemistry of Fe(II) oxidation in a photosynthetic microbial mat: implications for precambrian Fe(II) oxidation. Geochim. Cosmochim. Acta 71, 4629-4643.
91. van der Meer, M. T., Schouten, S., de Leeuw, J. W., and Ward, D. M. (2000). Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopically heavy organic carbon in the geological record. Environ. Microbiol. 2, 428-435.
92. van der Meer, M. T. J., Klatt, C. G., Wood, J., Bryant, D. A., Bateson, M. M., Lammerts, L., et al. (2010). Cultivation and genomic, nutritional, and lipid biomarker characterization of Roseiflexus strains closely related to predominant in situ populations inhabiting Yellowstone hot spring microbial mats. J. Bacteriol. 192, 3033-3042.
93. van der Meer, M. T. J., Schouten, S., Bateson, M. M., Nübel, U., Wieland, A., Kuhl, M., et al. (2005). Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone National Park. Appl. Environ. Microbiol. 71, 3978-3986.
94. van der Meer, M. T. J., Schouten, S., Sinninghe Damste, J. S., de Leeuw, J. W., and Ward, D. M. (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.
95. van Niel, C. B., and Thayer, L. A. (1930). Report on Preliminary Observations on the Microflora in and Near the Hot Springs in Yellowstone National Park and Their Importance for the Geological Formations. YNP Lib File 731.2, Mammoth, WY.
96. van Ooteghem, S. A., Jones, A., Van Der Lelie, D., Dong, B., and Mahajan, D. (2004). H2 production and carbon utilization by Thermotoga neapolitana under anaerobic and microaerobic growth conditions. Biotechnol. Lett. 26, 1223-1232.
97. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267.
98. Ward, D. M., and Castenholz, R. W. (2000). "Cyanobacteria in geothermal habitats," in Ecology of Cyanobacteria, eds B. A. Whitton, and M. Potts (Dordrecht: Kluwer Academic Publishers), 37-59.
99. Ward, D. M., Castenholz, R. W., and Miller, S. R. (2012). "Cyanobacteria in geothermal habitats," in Ecology of cyanobacteria II. Their diversity in space and time, ed. B. A. Whitton (Heidelberg, GE: Springer), 39-63.
100. Ward, D. M., Cohan, F. M., Bhaya, D., Heidelberg, J. F., Kühl, M., and Grossman, A. (2008). Genomics, environmental genomics and the issue of microbial species. Heredity 100, 207-219.
101. Ward, D. M., Ferris, M. J., Nold, S. C., and Bateson, M. M. (1998). A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol. Mol. Biol. Rev. 62, 1353-1370.
102. Ward, D. M., Weller, R., Shiea, J., Castenholz, R. W., and Cohen, Y. (1989). "Hot spring microbial mats: anoxygenic and oxygenic mats of possible evolutionary significance," in Microbial Mats: Physiological Ecology of Benthic Microbial Communities, eds Y. Cohen, and E. Rosenberg (Washington, DC: American Society of Microbiology), 3-15.
103. Wu, M., and Eisen, J. (2008). A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9, R151.
104. Zarzycki, J., and Fuchs, G. (2011). Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl. Environ. Microbiol. 77, 6181-6188.
105. Zeikus, J. G., and Wolfe, R. S. (1972). Methanobacterium thermoautotrophicus sp. n., an anaerobic, autotrophic, extreme thermophile. J. Bacteriol. 109, 707-713.