Deep-sea hydrothermal vent Epsilonproteobacteria encode a conserved and widespread nitrate reduction pathway (Nap)

ISME Journal

Volumn 8, Issue 7, 2014, Pages 1510-1521

  Vetriani, Costantino ^a   Voordeckers, James W ^a   Crespo Medina, Melitza ^a   O'Brien, Charles E ^a   Giovannelli, Donato ^a,b   Lutz, Richard A ^a  

^a RUTGERS UNIVERSITY   (United States)

^b CNR   (Italy)

Author keywords

deep sea vents; Epsilonproteobacteria; napA; nitrate reduction

Indexed keywords

BACTERIUM; DEEP SEA; GENE EXPRESSION; HYDROTHERMAL VENT COMMUNITY; MICROBIAL COMMUNITY; NITRATE; REDUCTION; RESPIRATION; SPECIES DIVERSITY;

BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA;

BACTERIAL PROTEIN; BACTERIAL RNA; NITRATE REDUCTASE; NITRIC ACID DERIVATIVE; RNA 16S;

ARTICLE; CLASSIFICATION; ECOSYSTEM; EPSILONPROTEOBACTERIA; GENETICS; HYDROTHERMAL VENT; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PHYLOGENY; TEMPERATURE;

BACTERIAL PROTEINS; ECOSYSTEM; EPSILONPROTEOBACTERIA; HYDROTHERMAL VENTS; NITRATE REDUCTASE; NITRATES; OXIDATION-REDUCTION; PHYLOGENY; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; TEMPERATURE;

EID: 84903391139     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.246     Document Type: Article

References (56)

1. Alain K, Zbinden M, Le Bris N, Lesongeur F, Querellou J, Gaill F et al. (2004). Early steps in microbial colonization processes at deep-sea hydrothermal vents. Environ Microbiol 6: 227-241. (Pubitemid 38261022
2. Blochl E, Rachel R, Burggraf S, Hafenbradl D, Jannasch HW, Stetter KO. (1997). Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 degrees C. Extremophiles 1: 14-21. (Pubitemid 127466763
3. Bourbonnais A, Juniper SK, Butterfield DA, Devol AH, Kuypers MMM, Lavik G et al. (2012a). Activity and abundance of denitrifying bacteria in the subsurface biosphere of diffuse hydrothermal vents of the Juan de Fuca Ridge. Biogeosciences 9: 4661-4678
4. Bourbonnais A, Lehmann MF, Butterfield DA, Juniper SK. (2012b). Subseafloor nitrogen transformations in diffuse hydrothermal vent fluids of the Juan de Fuca Ridge evidenced by the isotopic composition of nitrate and ammonium. Geochem Geophys Geosyst 13: Q02T01
5. Bru D, Sarr A, Philippot L. (2007). Relative abundances of proteobacterial membrane-bound and periplasmic nitrate reductases in selected environments. Appl Environ Microbiol 73: 5971-5974. (Pubitemid 47463015
6. Campbell BJ, Engel AS, Porter ML, Takai K. (2006). The versatile epsilon-proteobacteria: Key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468. (Pubitemid 43771865
7. Campbell BJ, Smith JL, Hanson TE, Klotz MG, Stein LY, Lee CK et al. (2009). Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet 5: E1000362
8. Cole J. (1996). Nitrate reduction to ammonia by enteric bacteria: Redundancy, or a strategy for survival during oxygen starvatioñ FEMS Microbiol Lett 136: 1-11
9. Dahle H, Roalkvam I, Thorseth IH, Pedersen RB, Steen IH. (2013). The versatile in situ gene expression of an Epsilonproteobacteria-dominated biofilm from a hydrothermal chimney. Environ Microbiol Rep 5: 282-290
10. Dong LF, Smith CJ, Papaspyrou S, Stott A, Osborn AM, Nedwell DB. (2009). Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Colne estuary, United Kingdom). Appl Environ Microbiol 75: 3171-3179
11. Flanagan DA, Gregory LG, Carter JP, Karakas-Sen A, Richardson DJ, Spiro S. (1999). Detection of genes for periplasmic nitrate reductase in nitrate respiring bacteria and in community DNA. FEMS Microbiol Lett 177: 263-270. (Pubitemid 29352223
12. Galtier N, Gouy M, Gautier C. (1996). SeaView and Phylo-win, two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548
13. Giovannelli D, Ferriera S, Johnson J, Kravitz S, Perez-Rodriguez I, Ricci J et al. (2011). Draft genome sequence of Caminibacter mediatlanticus strain TB-2(T), an epsilonproteobacterium isolated from a deep-sea hydrothermal vent. Stand Genomic Sci 5: 135-143
14. Grove J, Tanapongpipat S, Thomas G, Griffiths L, Crooke H, Cole J. (1996). Escherichia coli K-12 genes essential for the synthesis of c-Type cytochromes and a third nitrate reductase located in the periplasm. Mol Microbiol 19: 467-481. (Pubitemid 26052134
15. Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K. (2003). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53: 1801-1805. (Pubitemid 37483835
16. Jannasch HW. (1995). Microbial interactions with hydrothermal fluids. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds). Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions. American Geophysical Union: Washington, DC, pp 273-296
17. Karl DM. (1995). Ecology of free-living, hydrothermal vent microbial communities. In: Karl DM (ed). The Microbiology of Deep-Sea Hydrothermal Vents. CRC Press, Inc.: Boca Raton, FL, pp 35-124
18. Kern M, Mager AM, Simon J. (2007). Role of individual nap gene cluster products in NapC-independent nitrate respiration of Wolinella succinogenes. Microbiology 153: 3739-3747. (Pubitemid 350168252
19. Kern M, Simon J. (2008). Characterization of the NapGH quinol dehydrogenase complex involved in Wolinella succinogenes nitrate respiration. Mol Microbiol 69: 1137-1152
20. Kern M, Simon J. (2009a). Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Bioph Acta 1787: 646-656
21. Kern M, Simon J. (2009b). Periplasmic nitrate reduction in Wolinella succinogenes: Cytoplasmic NapF facilitates NapA maturation and requires the menaquinol dehydrogenase NapH for membrane attachment. Microbiology 155: 2784-2794
22. Le Bris N, Govenar B, Le Gall C, Fisher CR. (2006). Variability of physico-chemical conditions in 9 degrees 500 N EPR diffuse flow vent habitats. Mar Chem 98: 167-182. (Pubitemid 43049922
23. Lentner C. (1984). Composition of blood. Geigy Scientific Tables. Ciba-Geigy Limited: Basel, pp 81
24. Lin JT, Stewart V. (1998). Nitrate assimilation by bacteria. Adv Microb Physiol 39: 379
25. Lopez-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D. (2003). Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5: 961-976. (Pubitemid 37181567
26. Luther 3rd GW, Rozan TF, TaillefertM, Nuzzio DB, DiMeo C, Shank TM et al. (2001). Chemical speciation drives hydrothermal vent ecology. Nature 410: 813-816. (Pubitemid 32303778
27. MillerWG, Parker CT, RubenfieldM,Mendz GL,WostenMM, Ussery DW et al. (2007). The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS One 2: E1358
28. Millero FJ. (1996). Micronutrients in the oceans. Chemical Oceanography, 2nd edn. CRC Press, Inc.: Boca Raton, FL, pp 281-305
29. Miroshnichenko ML, Kostrikina NA, L'Haridon S, Jeanthon C, Hippe H, Stackebrandt E et al. (2002). Nautilia lithotrophica gen. nov., sp nov., a thermophilic sulfur-reducing epsilon-proteobacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 52: 1299-1304. (Pubitemid 34846430
30. Miroshnichenko ML, L'Haridon S, Schumann P, Spring S, Bonch-Osmolovskaya EA, Jeanthon C et al. (2004). Caminibacter profundus sp. nov., a novel thermophile of Nautiliales ord. nov. within the class 'Epsilonproteobacteria', isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 54: 41-45
31. Moreno-Vivian C, Cabello P, Martinez-Luque M, Blasco R, Castillo F. (1999). Prokaryotic nitrate reduction: Molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181: 6573-6584. (Pubitemid 29517969
32. Nakagawa S, Takai K, Inagaki F, Horikoshi K, Sako Y. (2005). Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the epsilon-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 55: 925-933. (Pubitemid 40485092
33. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K. (2007). Deep-sea vent E-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104: 12146-12150. (Pubitemid 47185644
34. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, Basham D et al. (2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668. (Pubitemid 30104008
35. Perez-Rodriguez I, Bohnert KA, Cuebas M, Keddis R, Vetriani C. (2013). Detection and phylogenetic analysis of the membrane-bound nitrate reductase (Nar) in pure cultures and microbial communities from deep-sea hydrothermal vents. FEMS Microbiol Ecol 86: 256-267
36. Perez-Rodriguez I, Grosche A, Massenburg L, Starovoytov V, Lutz RA, Vetriani C. (2012). Phorcysia thermohydrogeniphila gen. nov., sp nov., a thermophilic, chemolithoautotrophic, nitrate-Ammonifying bacterium from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 62: 2388-2394
37. Perez-Rodriguez I, Ricci J, Voordeckers JW, Starovoytov V, Vetriani C. (2010). Nautilia nitratireducens sp. nov., a thermophilic, anaerobic, chemosynthetic, nitrate-Ammonifying bacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 60: 1182-1186
38. Potter L, Angove H, Richardson D, Cole J. (2001). Nitrate reduction in the periplasm of gram-negative bacteria. Adv Microb Physiol 45: 51-112. (Pubitemid 32612190
39. Potter LC, Millington P, Griffiths L, Thomas GH, Cole JA. (1999). Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: Does Nap confer a selective advantage during nitrate-limited growth? Biochem J 344(Pt 1): 77-84
40. Reysenbach A-L, Gotz D, Yernool D. (2002). Microbial diversity of marine and terrestrial thermal springs. Biodiversity of Microbial Life. Wiley-Liss, Inc.: New York, NY, pp 345-421
41. Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ. (2001). Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58: 165-178. (Pubitemid 32217349
42. Sievert SM, Scott KM, Klotz MG, Chain PS, Hauser LJ, Hemp J et al. (2008). Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74: 1145-1156. (Pubitemid 351287086
43. Sikorski J, Munk C, Lapidus A, Ngatchou Djao OD, Lucas S, Glavina Del Rio T et al. (2010). Complete genome sequence of Sulfurimonas autotrophica type strain (OK10). Stand Genomic Sci 3: 194-202
44. Simon J, Sanger M, Schuster SC, Gross R. (2003). Electron transport to periplasmic nitrate reductase (NapA) of Wolinella succinogenes is independent of a NapC protein. Mol Microbiol 49: 69-79. (Pubitemid 36792004
45. Smith CJ, Nedwell DB, Dong LF, Osborn AM. (2007). Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73: 3612-3622. (Pubitemid 46871451
46. Smith JL, Campbell BJ, Hanson TE, Zhang CL, Cary SC. (2008). Nautilia profundicola sp. nov., a thermophilic, sulfur-reducing epsilonproteobacterium from deepsea hydrothermal vents. Int J Syst Evol Microbiol 58: 1598-1602
47. Suerbaum S, Josenhans C, Sterzenbach T, Drescher B, Brandt P, Bell M et al. (2003). The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci USA 100: 7901-7906. (Pubitemid 36760067
48. Takai K, Inagaki F, Nakagawa S, Hirayama H, Nunoura T, Sako Y et al. (2003). Isolation and phylogenetic diversity of members of previously uncultivated E-Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiol Lett 218: 167-174. (Pubitemid 36173544
49. Takai K, Nealson KH, Horikoshi K. (2004). Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the epsilon-Proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. Int J Syst Evol Microbiol 54: 25-32. (Pubitemid 38181267
50. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F et al. (2006). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen-And sulfuroxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56: 1725-1733. (Pubitemid 44288391
51. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. (1997). The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882. (Pubitemid 28022245
52. Vetriani C, Speck MD, Ellor SV, Lutz RA, Starovoytov V. (2004). Thermovibrio ammonificans sp. nov., a thermophilic, chemolithotrophic, nitrate ammonifying bacterium from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 54: 175-181. (Pubitemid 38181287
53. Vetriani C, Tran HV, Kerkhof LJ. (2003). Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl Environ Microbiol 69: 6481-6488. (Pubitemid 37420180
54. Voordeckers J, Starovoytov V, Vetriani C. (2005). Caminibacter mediatlanticus sp. nov., a thermophilic, chemolithoautotrophic, nitrate ammonifying bacterium isolated from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. Int J Syst Evol Microbiol 55: 773-779. (Pubitemid 40485069
55. Voordeckers JW, Do M, Hügler M, Ko V, Sievert SM, Vetriani C. (2008). Culture dependent and independent analyses of 16S rRNA and ATP citrate lyase genes: A comparison of microbial communities from different black smoker chimneys on the Mid-Atlantic Ridge. Extremophiles 12: 627-640
56. Wang H, Tseng CP, Gunsalus RP. (1999). The napF and narG nitrate reductase operons in Escherichia coli are differentially expressed in response to submicromolar concentrations of nitrate but not nitrite. J Bacteriol 181: 5303-5308. (Pubitemid 29416350