Phototrophic Phylotypes Dominate Mesothermal Microbial Mats Associated with Hot Springs in Yellowstone National Park

Microbial Ecology

Volumn 64, Issue 1, 2012, Pages 162-170

  Ross, Kimberly A ^a   Feazel, Leah M ^a,b   Robertson, Charles E ^a   Fathepure, Babu Z ^c   Wright, Katherine E ^a   Turk MacLeod, Rebecca M ^a,d   Chan, Mallory M ^a,b   Held, Nicole L ^a,e   Spear, John R ^f   Pace, Norman R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c OKLAHOMA STATE UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^f Department of Metallurgical and Materials Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S;

ARTICLE; BACTERIUM; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOTOTROPHY; PHYLOGENY; THERMAL SPRING; UNITED STATES;

BACTERIA; COLORADO; DNA, BACTERIAL; HOT SPRINGS; MOLECULAR SEQUENCE DATA; PHOTOTROPHIC PROCESSES; PHYLOGENY; RNA, RIBOSOMAL, 16S;

ACIDOBACTERIUM; BACTERIA (MICROORGANISMS); CHLOROBI; CHLOROFLEXI; CHLOROFLEXI (CLASS); CYANOBACTERIA; THERMOPHILUM;

EID: 84862496781     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-012-0012-3     Document Type: Article

References (52)

1. Brock TD (1978) Thermophilic microorganisms and life at high temperatures. Springer, New York.
2. Ferris MJ, Magnuson TS, Fagg JA, Thar R, Kühl M, Sheehan KB, Henson JM (2003) Microbially mediated sulphide production in a thermal, acidic algal mat community in Yellowstone National Park. Environ Microbiol 5: 954-960.
3. Ward DM and FM Cohan (2005) Microbial diversity in hot spring cyanobacterial mats: pattern and prediction, geothermal biology and geochemistry in Yellowstone National Park: Proceeding of the Thermal Biology Institute Workshop, Yellowstone National Park, WY., pp. 185-202 Montana State University Publications.
4. Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci USA 102: 2555-2560.
5. Walker JJ, Spear JR, Pace NR (2005) Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434: 1011-1014.
6. Brock TD, Freeze H (1969) Thermus aquaticus gen. n. and sp. n., a nonsporulating extreme thermophile. J Bacteriol 98: 289-297.
7. Reysenbach AL, Wickham GS, Pace NR (1994) Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. Appl Environ Microbiol 60: 2113-2119.
8. Huber R, Eder W, Heldwein S, Wanner G, Huber H, Rachel R, Stetter KO (1998) Thermocrinis ruber gen. nov., sp. nov., a pink-filament-forming hyperthermophilic bacterium isolated from Yellowstone National Park. Appl Environ Microbiol 64: 3576-3583.
9. Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180: 366-376.
10. Castenholz RW, Ward DM (2000) Cyanobacteria in geothermal habitats, the ecology of cyanobacteria: their diversity in time and space. Springer, Berlin, pp 37-59.
11. Boomer SM, Lodge DP, Dutton BE, 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.
12. Johnson DB, Okibe N, Roberto FF (2003) Novel thermo-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics. Arch Microbiol 180: 60-68.
13. Jaenicke R and R Sterner (2006) Life at high temperatures. The Prokaryotes, pp. 167-209.
14. Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR (2001) Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ Microbiol 3: 532-542.
15. Langner HW, Jackson CR, McDermott TR, Inskeep WP (2001) Rapid oxidation of arsenite in a hot spring ecosystem, Yellowstone National Park. Environ Sci Technol 35: 3302-3309.
16. Nordstrom DK, Ball JW, and McCleskey RB (2005) Ground water to surface water: chemistry of thermal outflows in Yellowstone National Park, geothermal biology and geochemistry in Yellowstone National Park: Proceeding of the Thermal Biology Institute Workshop, Yellowstone National Park, WY., pp. 73-94 Montana State University Publications.
17. Inskeep WP, Rusch DB, Jay ZJ, Herrgard MJ, Kozubal MA, Richardson TH, Macur RE, Hamamura N, Jennings R, Fouke BW, Reysenbach A-L, Roberto F, Young M, Schwartz A, Boyd ES, Badger JH, Mathur EJ, Ortmann AC, Bateson M, Geesey G, Frazier M (2010) Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS One 5: e9773.
18. Jackson TJ, Ramaley RF, Meinschein WG (1973) Thermomicrobium, a new genus of extremely thermophilic bacteria. Int J Syst Bacteriol 23: 28-36.
19. Pierson BK, Castenholz RW (1974) A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100: 5-24.
20. Allewalt JP, Bateson MM, Revsbech NP, Slack K, Ward DM (2006) Effect of temperature and light on growth of and photosynthesis by synechococcus isolates typical of those predominating in the Octopus Spring microbial mat community of Yellowstone National Park. Appl Environ Microbiol 72: 544-550.
21. Bryant DA, Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317: 523-526.
22. van der Meer MTJ, Klatt CG, Wood J, Bryant DA, Bateson MM, Lammerts L, Schouten S, Sinninghe Damste JS, Madigan MT, Ward DM (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.
23. Ferris M, Ward D (1997) Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis. Appl Environ Microbiol 63: 1375-1381.
24. Miller SR, Strong AL, Jones KL, Ungerer MC (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.
25. Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5: 650-659.
26. Boomer SM, Noll KL, Geesey GG, and BE Dutton (2009) Formation of multilayered photosynthetic biofilms in an alkaline thermal spring in Yellowstone National Park, WY, USA. Appl. Environ. Microbiol. AEM. 01802-08.
27. Ward DM, Bateson MM, Ferris MJ, Kühl M, Wieland A, Koeppel A, Cohan FM (2006) Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function. Philos Trans R Soc London Series B, Biological Sciences 361: 1997-2008.
28. Stahl DA, Lane DJ, Olsen GJ, Pace NR (1985) Characterization of a Yellowstone hot spring microbial community by 5S rRNA sequences. Appl Environ Microbiol 49: 1379-1384.
29. Ward DM, Weller R, Bateson MM (1990) 16S rRNA sequences reveal uncultured inhabitants of a well-studied thermal community. FEMS Microbiol Rev 6: 105-115.
30. Steunou A-S, Bhaya D, Bateson MM, Melendrez MC, Ward DM, Brecht E, Peters JW, Kühl M, Grossman AR (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci USA 103: 2398-2403.
31. Kilian O, Steunou A-S, Fazeli F, Bailey S, Bhaya D, Grossman AR (2007) Responses of a thermophilic synechococcus isolate from the microbial mat of Octopus Spring to light. Appl Environ Microbiol 73: 4268-4278.
32. Bhaya D, Grossman AR, Steunou A-S, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Bateson MM, Ward DM, Heidelberg JF (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1: 703-713.
33. Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64: 3869-3877.
34. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci 82: 6955-6959.
35. Frank D (2008) XplorSeq: a software environment for integrated management and phylogenetic analysis of metagenomic sequence data. BMC Bioinformatics 9: 420.
36. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
37. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar A, Buchner T, Lai S, Steppi G, Jobb W, Förster I, Brettske S, Gerber AW, Ginhart O, Gross S, Grumann S, Hermann R, Jost A, König T, Liss R, Lüßmann M, May B, Nonhoff B, Reichel R, Strehlow A, Stamatakis N, Stuckmann A, Vilbig M, Lenke T, Ludwig AB, Schleifer K (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
38. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11: 265-270.
39. Kemp PF, Aller JY (2004) Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. Ecol FEMS Microbiol 47: 161-177.
40. Magurran AE (2004) Measuring biological diversity. Blackwell Publishing Company, Boston.
41. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinforma (Oxf, Engl) 21: 456-463.
42. Kuczynski J, Costello EK, Nemergut DR, Zaneveld J, Lauber CL, Knights D, Koren O, Fierer N, Kelley ST, Ley RE, Gordon JI, Knight R (2010) Direct sequencing of the human microbiome readily reveals community differences. Genome Biol 11: 210.
43. Ferris M, Ruff-Roberts A, Kopczynski E, Bateson M, Ward D (1996) Enrichment culture and microscopy conceal diverse thermophilic synechococcus populations in a single hot spring microbial mat habitat. Appl Environ Microbiol 62: 1045-1050.
44. Ramsing NB, Ferris MJ, Ward DM (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.
45. Xia Y, Kong Y, Nielsen PH (2007) In situ detection of protein-hydrolysing microorganisms in activated sludge. FEMS Microbiol Ecol 60: 156-165.
46. de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10: 810-818.
47. Spear JR, Ley RE, Berger AB, Pace NR (2003) Complexity in natural microbial ecosystems: the Guerrero Negro experience. Biol Bull 204: 168-173.
48. Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72: 3685-3695.
49. Feazel LM, Spear JR, Berger AB, Harris JK, Frank DN, Ley RE, Pace NR (2008) Eucaryotic diversity in a hypersaline microbial mat. Appl Environ Microbiol 74: 329-332.
50. Robertson CE, Spear JR, Harris JK, Pace NR (2009) Diversity and stratification of Archaea in a hypersaline microbial mat. Appl Environ Microbiol 75: 1801-1810.
51. Valiela I (1995) Marine ecological processes. Springer, Berlin.
52. Baumgartner LK, Dupraz C, Buckley DH, Spear JR, Pace NR, Visscher PT (2009) Microbial species richness and metabolic activities in hypersaline microbial mats: insight into biosignature formation through lithification. Astrobiology 9: 861-874.