Niche differentiation among sulfur-oxidizing bacterial populations in cave waters

ISME Journal

Volumn 2, Issue 6, 2008, Pages 590-601

  Macalady, Jennifer L ^a   Dattagupta, Sharmishtha ^a   Schaperdoth, Irene ^a   Jones, Daniel S ^a   Druschel, Greg K ^b   Eastman, Danielle ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Beggiatoa; Epsilonproteobacteria; Frasassi cave; Microelectrode voltammetry; Thiothrix; Thiovirga

Indexed keywords

BACTERIAL DNA; OXYGEN; RIBOSOME DNA; RNA 16S; SULFUR; WATER;

ARTICLE; BIOFILM; CLASSIFICATION; DNA SEQUENCE; EPSILONPROTEOBACTERIA; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; ITALY; METABOLISM; MICROBIOLOGY; PHYLOGENY;

BIOFILMS; DNA, BACTERIAL; DNA, RIBOSOMAL; EPSILONPROTEOBACTERIA; GENE LIBRARY; ITALY; OXYGEN; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SULFUR; WATER; WATER MICROBIOLOGY;

BACTERIA (MICROORGANISMS); BEGGIATOA; EPSILONPROTEOBACTERIA; THIOTHRIX; THIOVIRGA;

EID: 44849139426     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2008.25     Document Type: Article

References (43)

1. Ahmad A, Kalanetra KM, Nelson DC. (2006). Cultivated Beggiatoa spp. define the phylogenetic root of morphologically diverse, noncultured, vacuolate sulfur bacteria. Can J Microbiol 52: 591-598.
2. Amann RI. (1995). In situ identification of microorganisms by whole cell hybridization with rRNA-targeted nucleic acid probes. Mol Microb Ecol Manual 3: 1-15.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. (1990). Basic local alignment search tools. J Mol Bio 215: 403-410.
4. Bond PL, Smriga SP, Banfield JF. (2000). Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microbiol 66: 3842-3849.
5. 2, and S(-Ii) in porewaters of marine and fresh-water sediments. Env Sci Technol 29: 751-761.
6. Campbell BJ, Engel AS, Porter ML, Takai K. (2006). The versatile ε-proteobacteria: key players in sulphidic habitats. Nature Rev Microbiol 4: 458-468.
7. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA et al. (2003). The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31: 442-443.
8. Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M. (1999). The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
9. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072.
10. Druschel GK, Hamers RJ, Luther GW, Banfield JF. (2003). Kinetics and mechanism of trithionate and tetrathio-nate oxidation at low pH by hydroxyl radicals. Aquatic Geochem 9: 145-164.
11. Druschel GK, Sutka R, Emerson D, Luther GW, Kraiya C, Glazer B. (2004). Voltammetric investigation of Fe-Mn-S species in a microbially active wetland. In: Wanty RB, Seal RR (eds). Eleventh International Symposium on Water-Rock Interaction WRI-11. Balk-ema: Saratoga Springs, NY, USA, pp 1191-1194.
12. Elshahed MS, Senko JM, Najar FZ, Kenton SM, Roe BA, Dewers TA et al. (2003). Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring. Appl Environ Microbiol 69: 5609-5621.
13. Engel AS, Lee N, Porter ML, Stern LA, Bennett PC, Wagner M. (2003). Filamentous 'Epsilonproteobacteria' dominate microbial mats from sulfidic cave springs. Appl Environ Microbiol 69: 5503-5511.
14. Engel AS, Porter ML, Stern LA, Quinlan S, Bennett PC. (2004). Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfi-dic springs dominated by chemolithoautotrophic 'Epsilonproteobacteria'. FEMS Microbiol Ecol 51: 31.
15. Galdenzi S, Cocchioni M, Morichetti L, Amici V, Scuri S. (2007). Sulfidic groundwater chemistry in the Frasassi caves, Italy. J Cave Karst (in press).
16. Glazer BT, Luther GW, Konovalov SK, Friederich GE, Nuzzio DB, Trouwborst RE et al. (2006). Documenting the suboxic zone of the Black Sea via high-resolution realtime redox profiling. Deep Sea Res II 53: 1740-1755.
17. Glazer BT, Marsh AG, Stierhoff K, Luther GW. (2004). The dynamic response of optical oxygen sensors and voltammetric electrodes to temporal changes in dissolved oxygen concentrations. Analyt Chim Acta 518: 93-100.
18. Huber T, Faulkner G, Hugenholtz P. (2004). Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
19. Hugenholtz P, Tyson GW, Blackall LL. (2001). Design and evaluation of 16S rRNA-targeted oligonucleotide probes for fluorescent in situ hybridization. In: de Muro MA, Rapley R (eds). Gene Probes: Principles and Protocols. Humana Press: London. pp 29-42.
20. Ito T, Sugita K, Yumoto I, Nodasaka Y, Okabe S. (2005). Thiovirga sulfuroxydans gen. nov., sp. nov., a chemo-lithoautotrophic sulfur-oxidizing bacterium isolated from a microaerobic waste-water biofilm. Int J Syst Evol Microbiol 55: 1059-1064.
21. Jones DS, Lyon EH, Macalady JL. (2008). Geomicrobiology of sulfidic cave biovermiculations. J Cave Karst (in press).
22. 2 and HS microgradients. Appl Environ Microbiol 45: 1261-1270.
23. Kalanetra KM, Huston SL, Nelson DC. (2004). Novel, attached, sulfur-oxidizing bacteria at shallow hydro-thermal vents possess vacuoles not involved in respiratory nitrate accumulation. Appl Environ Microbiol 70: 7487-7496.
24. Lane DJ. (1991). 16S/23S rRNA sequencing. In: Stack-ebrandt E, Goodfellow M (eds). 1Nucleic Acid Techniques in Bacterial Systematics. Wiley: New York. pp 115-175.
25. 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.
26. 2∼) and porewater parameters in salt-marsh sediments. Biogeochem 14: 57-88.
27. Luther GW, Glazer BT, Hohmann L, Popp JI, Taillefert M, Rozan TF et al. (2001). Sulfur speciation monitored in situ with solid state gold amalgam voltammetric microelectrodes: polysulfides as a special case in sediments, microbial mats and hydrothermal vent waters. J Environ Monitoring 3: 61-66.
28. Macalady JL, Jones DS, Lyon EH. (2007). Extremely acidic, pendulous microbial biofilms from the Frasassi cave system, Italy. Environ Microbiol 9: 1402-1414.
29. Macalady JL, Lyon EH, Koffman B, Albertson LK, Meyer K, Galdenzi S et al. (2006). Dominant microbial populations in limestone-corroding stream biofilms, Frasassi cave system, Italy. Appl Environ Microbiol 72: 5596-5609.
30. Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H. (1992). Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593-600.
31. Nielsen PH, de Muro MA, Nielsen JL. (2000). Studies on the in situ physiology of Thiothrix spp. present in activated sludge. Environ Microbiol 2: 389-398.
32. Preisler A, de Beer D, Lichtschlag A, Lavik G, Boetius A, Jorgensen BB. (2007). Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1: 341.
33. Sarbu S, Galdenzi S, Menichetti M, Gentile G. (2000). Geology and biology of the Frasassi caves in central Italy: an ecological multi-disciplinary study of a hypogenic underground karst system. In: Wilkens H (ed). Ecosystems of the World. Elsevier: New York, NY. pp 359-378.
34. Schulz HN, Jorgensen BB. (2001). Big bacteria. Annu Rev Microbiol 55: 105-137.
35. Skoog D, Holler F, Neiman T. (1998). Principles of Instrumental Analysis, 5. Brooks/Cole-Thomas Learning. Pacific Grove: CA.
36. Stahl DA, Amann R. (1991). Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds). Nucleic acid techniques in bacterial systema-tics. John Wiley & Sons Ltd: Chichester, England, pp 205-248.
37. St Maurice M, Cremades N, Croxen MA, Sisson G, Sancho J, Hoffman PS. (2007). Flavodoxin:quinone reductase (FqrB): a redox partner of pyruvate:ferredoxin oxidor-eductase that reversibly couples pyruvate oxidation to NADPH production in Helicobacter pylori and Cam-pylobacter jejuni. J Bacteriol 189: 4764-4773.
38. Swofford DL. (2000). PAUP*: Phylogenetic Analysis Using Parsimony and Other Methods (Software). Sinauer Associates: Sunderland, MA.
39. Taillefert M, Bono AB, Luther GW. (2000). Reactivity of freshly formed Fe(III) in synthetic solutions and (pore)waters: voltammetric evidence of an aging process. Env Sci Technol 34: 2169-2177.
40. Taillefert M, Rozan TF. (2002). Electrochemical methods for the environmental analysis of trace elements biogeochemistry. In: Taillefert M, Rozan TF (eds). Environmental Electrochemistry: Analyses of Trace Element Biogeochemistry. American Chemical Society: Washington DC, pp 3-14.
41. Vlasceanu L, Sarbu SM, Engel AS, Kinkle BK. (2000). Acidic cave wall biofilms located in the Frasassi Gorge, Italy. Geomicrobiol J 17: 125-139.
42. Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad A, Taylor LT et al. (2002). Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68: 316-325.
43. Xu K, Dexter SC, Luther GW. (1998). Voltammetric microelectrodes for biocorrosion studies. Corrosion 54: 814-823.