Metagenomic Evidence for Sulfide Oxidation in Extremely Acidic Cave Biofilms

Geomicrobiology Journal

Volumn 31, Issue 3, 2014, Pages 194-204

  Jones, Daniel S ^a   Schaperdoth, Irene ^a   Macalady, Jennifer L ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

archaea; biofilm; community structure; hydrogen sulfide; karst; subsurface microbiology

Indexed keywords

BIOFILM; CAVE; COMMUNITY COMPOSITION; HYDROGEN SULFIDE; KARST; MICROBIAL COMMUNITY; OXIDATION;

EID: 84893276179     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490451.2013.834008     Document Type: Article

References (53)

1. Abascal, F, Zardoya, R and Posada, D. 2005. ProtTest: Selection of best-fit models of protein evolution. Bioinformatics, 21: 2104 - 2105.
2. Altschul, S, Madden, T, Schäffer, A, Zhang, J, Zhang, Z, Miller, W and Lipman, D. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucl Acids Res, 25: 3389 - 3402.
3. Armougom, F, Moretti, S, Poirot, O, Audic, S, Dumas, P, Schaeli, B, Keduas, V and Notredame, C. 2006. Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucl Acids Res, 34: W604 - W608.
4. Baker, B J and Banfield, J F. 2003. Microbial communities in acid mine drainage. FEMS Microbiol Ecol, 44: 139 - 152.
5. Berg, I A, Kockelkorn, D, Ramos-Vera, W H, Say, R F, Zarzycki, J, Hügler, M, Alber, B E and Fuchs, G. 2010. Autotrophic carbon fixation in archaea. Nat Rev Microbiol, 8: 447 - 460.
6. Brito, J A, Sousa, F L, Stelter, M, Bandeiras, T M, Vonrhein, C, Teixeira, M, Pereira, M M and Archer, M. 2009. Structural and functional insights into sulfide:quinone oxidoreductase. Biochemistry, 48: 5613 - 5622.
7. 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.
8. Chen, L X, Ren, Y L, Lin, J Q, Liu, X M and Pang, X. 2012. Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One, 7: e39470
9. Chen, Z W, Koh, M, Van Driessche, G, Van Beeumen, J J, Bartsch, R G, Meyer, T E, Cusanovich, M A and Mathews, F S. 1994. The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science, 266: 430 - 432.
10. Cherney, M M, Zhang, Y, Solomonson, M, Weiner, J H and James, M NG. 2010. Crystal structure of sulfide: quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol, 398: 292 - 305.
11. Chevreux, B, Wetter, T and Suhai, S. 1999. Genome sequence assembly using trace signals and additional sequence information. In: Proceedings of the German Conference on Bioinformatics (GCB) 99, Hanover, Germany,: 45 - 56.
12. Ciccarelli, F, Doerks, T, Von Mering, C, Creevey, C, Snel, B and Bork, P. 2006. Toward automatic reconstruction of a highly resolved tree of life. Science, 311: 1283 - 1287.
13. Dattagupta, S, Schaperdoth, I, Montanari, A, Mariani, S, Kita, N, Valley, J W and Macalady, J L. 2009. A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. ISME J, 3: 935 - 943.
14. DeSantis, T Z, Hugenholtz, P, Larsen, N, Rojas, M, Brodie, E L, Keller, K, Huber, T D.D, Hu, P and Anderson, G L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol, 72: 5069 - 5072.
15. Dick, G J, Andersson, A F, Baker, B J, Simmons, S L, Thomas, B C, Yelton, A P and Banfield, J F. 2009. Community-wide analysis of microbial genome sequence signatures. Genome Biol, 10: R85
16. Dopson, M and Johnson, D B. 2012. Biodiversity, metabolism and applications of acidophilic sulfur-metabolizing microorganisms. Environ Microbiol, 14: 2620 - 2631.
17. Druschel, G, Baker, B, Gihring, T and Banfield, J. 2004. Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem Trans, 5: 13 - 32.
18. Felsenstein, J. 1989. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics, 5: 164 - 166.
19. Golyshina, O V, Pivovarova, T A, Karavaiko, G I, Kondrat'eva, T F, Moore, E, Abraham, W R, Lünsdorf, H, Timmis, K N, Yakimov, M M and Golyshin, P. 2000. Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol, 50: 997 - 1006.
20. Gordon, D, Abajian, C and Green, P. 1998. Consed: a graphical tool for sequence finishing. Genome Res, 8: 195 - 202.
21. 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: 1 - 14.
22. Griesbeck, C, Schütz, M, Schödl, T, Bathe, S, Nausch, L, Mederer, N, Vielreicher, M and Hauska, G. 2002. Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry, 41: 11552 - 11565.
23. Hose, L D, Palmer, A N, Palmer, M V, Northup, D E, Boston, P J and DuChene, H R. 2000. Microbiology and geochemistry in a hydrogen-sulphide-rich karst environment. Chem Geol, 169: 399 - 423.
24. Huber, T, Faulkner, G and Hugenholtz, P. 2004. Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics, 20: 2317 - 2319.
25. Johnson, D B and Hallberg, K B. 2008. Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Adv Microb Physiol, 54: 201 - 255.
26. Jones, D, Lyon, E and Macalady, J. 2008. Geomicrobiology of biovermiculations from the Frasassi cave system, Italy. J Cave Karst Stud, 70: 78 - 93.
27. Jones, D, Tobler, D, Schaperdoth, I, Mainiero, M and Macalady, J. 2010. Community structure of subsurface biofilms in the thermal sulfidic caves of Acquasanta Terme, Italy. Appl Environ Microbiol, 76: 5902 - 5910.
28. Jones, D S, Albrecht, H L, Dawson, K S, Schaperdoth, I, Freeman, K H, Pi, Y, Pearson, A and Macalady, J L. 2012. Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm. ISME J, 6: 158 - 170.
29. Kelly, D and Wood, A. 2000. Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol, 50: 511 - 516.
30. Le, S Q and Gascuel, O. 2008. An improved general amino acid replacement matrix. Mol Biol Evol, 25: 1307 - 1320.
31. Lencina, A M, Ding, Z, Schurig-Briccio, L A and Gennis, R B. 2013. Characterization of the Type III sulfide:quinone oxidoreductase from Caldivirga maquilingensis and its membrane binding. BBA-Bioenergetics, 1827: 266 - 275.
32. Ludwig, W, Strunk, O, Westram, R, Richter, L, Meier, H, Yadhukumar, Buchner, A, Lai, T, Steppi, S, Jobb, G, Förster, W, Brettske, I, Gerber, S, Ginhart, A W, Gross, O, Grumann, S, Hermann, S, Jost, R, König, A, Liss, T, Lüßmann, R, May, M, Nonhoff, B, Reichel, B, Strehlow, R, Stamatakis, A, Stuckmann, N, Vilbig, A, Lenke, M, Ludwig, T, Bode, A and Schleifer, K-H. 2004. ARB: a software environment for sequence data. Nucl Acids Res, 32: 1363 - 1371.
33. Macalady, J L, Dattagupta, S, Schaperdoth, I, Jones, D S, Druschel, G K and Eastman, D. 2008. Niche differentiation among sulfur-oxidizing bacterial populations in cave waters. ISME J, 2: 590 - 601.
34. Macalady, J L, Jones, D S and Lyon, E H. 2007. Extremely acidic, pendulous microbial biofilms from the Frasassi cave system, Italy. Environ Microbiol, 9: 1402 - 1414.
35. Macalady, J L, Lyon, E H, Koffman, B, Albertson, L K, Meyer, K, Galdenzi, S and Mariani, S. 2006. Dominant microbial populations in limestone-corroding stream biofilms, Frasassi cave system, Italy. Appl Environ Microbiol, 72: 5596 - 5609.
36. Mangold, S, Valdés, J, Holmes, D S and Dopson, M. 2011. Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front Microbiol, 2: 17
37. 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 USA, 106: 9625 - 9630.
38. Marcia, M, Ermler, U, Peng, G and Michel, H. 2010. A new structure-based classification of sulfide:quinone oxidoreductases. Proteins, 78: 1073 - 1083.
39. Markowitz, V, Ivanova, N, Szeto, E, Palaniappan, K, Chu, K, Dalevi, D, Chen, I, Min, A, Grechkin, Y and Dubchak, I. 2007. IMG/M: a data management and analysis system for metagenomes. Nucleic Acids Res, 36: D534 - 538.
40. Matsen, F A, Kodner, R B and Armbrust, E V. 2010. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics, 11: 538
41. McCune, B and Grace, J B. 2002. Analysis of Ecological Communities, Gleneden Beach, Oregon: MjM Software Design.
42. Pruesse, E, Quast, C, Knittel, K, Fuchs, B M, Ludwig, W, Peplies, J and Glöckner, F O. 2007. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucl Acids Res, 35: 7188 - 7196.
43. R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: ISBN 3-900051-07-0. URL http://www.R-project.org/
44. Rice, P, Longden, I and Bleasby, A. 2000. EMBOSS: the European molecular biology open software suite. Trends Genet, 16: 276 - 277.
45. Rohwerder, T and Sand, W. 2007. Oxidation of inorganic sulfur compounds in acidophilic prokaryotes. Eng Life Sci, 7: 301 - 309.
46. Sagredo, B, Jedlicki, E and Orellana, O. 1992. Organization of the 16S-23S intergenic spacer region of the two rRNA operons from Thiobacillus ferrooxidans. Geomicrobiol J, 10: 239 - 247.
47. Sarbu, S M, Galdenzi, S, Menichetti, M and 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 Ecosystems of the World, Edited by: Wilkens, H, Culver, D and Humphreys, W. Vol. 30, p359 - 378. New York: Elsevier.
48. Schmieder, R and Edwards, R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics, 27: 863 - 864.
49. Simpson, J T and Durbin, R. 2012. Efficient de novo assembly of large genomes using compressed data structures. Genome Res, 22: 549 - 556.
50. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2688 - 2690.
51. 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.
52. Veith, A, Urich, T, Seyfarth, K, Protze, J, Frazão, C and Kletzin, A. 2011. Substrate pathways and mechanisms of inhibition in the sulfur oxygenase reductase of Acidianus ambivalens. Front Microbiol, 2
53. Vlasceanu, L, Sarbu, S M, Engel, A S and Kinkle, B K. 2000. Acidic cave wall biofilms located in the Frasassi Gorge, Italy. Geomicrobiol J, 17: 125 - 139.