Detection and phylogenetic analysis of the membrane-bound nitrate reductase (Nar) in pure cultures and microbial communities from deep-sea hydrothermal vents

FEMS Microbiology Ecology

Volumn 86, Issue 2, 2013, Pages 256-267

  Pérez Rodríguez, Ileana ^a,b   Bohnert, Kenneth A ^a,c   Cuebas, Mariola ^a   Keddis, Ramaydalis ^a   Vetriani, Costantino ^a  

^a RUTGERS UNIVERSITY   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anaerobic respiration; Bacteria; Deep sea; Hydrothermal fluids; Nitrate reduction; Nitrogen cycle

Indexed keywords

NITRATE REDUCTASE; RNA 16S;

CLONE; DEEP SEA; ENZYME; GENE; HYDROTHERMAL VENT; HYDROTHERMAL VENT COMMUNITY; MICROBIAL COMMUNITY; NITROGEN CYCLE; PHYLOGENETICS; RESPIRATION; SEAWATER;

ANAEROBIC RESPIRATION; ARTICLE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; DEEP-SEA; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENETICS; HYDROTHERMAL FLUIDS; HYDROTHERMAL VENT; ISOLATION AND PURIFICATION; MICROBIOLOGY; NITRATE REDUCTION; NITROGEN CYCLE; PHYLOGENY; PROTEOBACTERIA; RNA GENE;

ANAEROBIC RESPIRATION; BACTERIA; DEEP-SEA; HYDROTHERMAL FLUIDS; NITRATE REDUCTION; NITROGEN CYCLE;

BACTERIA; BIODIVERSITY; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENES, RRNA; HYDROTHERMAL VENTS; NITRATE REDUCTASE; PHYLOGENY; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S;

ATLANTIC OCEAN; EAST PACIFIC RISE; MID-ATLANTIC RIDGE; PACIFIC OCEAN;

BACTERIA (MICROORGANISMS); EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; MARINOBACTER;

EID: 84885952970     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12158     Document Type: Article

References (54)

1. Alain K, Querellou J, Lesongeur F, Pignet P, Crassous P, Raguenes G, Cueff V & Cambon-Bonavita MA (2002) Caminibacter hydrogeniphilus gen. nov., sp nov., a novel thermophilic, hydrogen-oxidizing bacterium isolated from an East Pacific Rise hydrothermal vent. Int J Syst Evol Microbiol 52: 1317-1323.
2. Alain K, Zbinden M, Le Bris N, Lesongeur F, Querellou J, Gaill F & Cambon-Bonavita MA (2004) Early steps in microbial colonization processes at deep-sea hydrothermal vents. Environ Microbiol 6: 227-241.
3. Alain K, Callac M, Guegan M, Lesongeur F, Crassous P, Cambon-Bonavita MA & Querellou J (2009) Nautilia abyssi sp. nov., a thermophilic, chemolithoautotrophic, sulfur-reducing bacterium isolated from an East Pacific Rise hydrothermal vent. Int J Syst Evol Microbiol 59: 1310-1315.
4. Alcantara-Hernandez RJ, Valenzuela-Encinas C, Marsch R & Dendooven L (2009) Respiratory and dissimilatory nitrate-reducing communities from an extreme saline alkaline soil of the former lake Texcoco. Extremophiles 13: 169-178.
5. Argandona M, Martinez-Checa F, Llamas I, Arco Y, Quesada E & del Moral A (2006) A membrane-bound nitrate reductase encoded by the narGHJI operon is responsible for anaerobic respiration in Halomonas maura. Extremophiles 10: 411-419.
6. Auclair J, Lepine F, Parent S & Villemur R (2010) Dissimilatory reduction of nitrate in seawater by a Methylophaga strain containing two highly divergent narG sequences. ISME J 10: 1302-1313.
7. Campbell BJ, Engel AS, Porter ML & Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468.
8. Campbell BJ, Smith JL, Hanson TE et al. (2009) Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genet 5: e1000362.
9. Cheneby D, Hallet S, Mondon M, Martin-Laurent F, Germon JC & Philippot L (2003) Genetic characterization of the nitrate reducing community based on narG nucleotide sequence analysis. Microb Ecol 46: 113-121.
10. Crespo-Medina M, Chatziefthimiou AD, Cruz-Matos R et al. (2009) Salinisphaera hydrothermalis sp. nov., a novel mesophilic, facultative chemotrophic Gammaproteobacterium from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 59: 1497-1503.
11. Drummond AJ, Ashton B, Buxton S et al. (2011) Geneious v5.4, Available at http://www.geneious.com/.
12. Falkowski PG, Fenchel T & Delong EF (2008) The microbial engines that drive Earth's biogeochemical cycles. Science 320: 1034-1039.
13. 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.
14. T, an Epsilonproteobacterium isolated from a deep-sea hydrothermal vent. Stand Genomic Sci 5: 135-143.
15. Girguis PR, Lee RW, Desaulniers N, Childress JJ, Pospesel M, Felbeck H & Zal F (2000) Fate of nitrate acquired by the tubeworm Riftia pachyptila. Appl Environ Microbiol 66: 2783-2790.
16. Götz D, Banta A, Beveridge TJ, Rushdi AI, Simoneit BR & Reysenbach AL (2002) Persephonella marina gen. nov., sp. nov. and Persephonella guaymasensis sp. nov., two novel, thermophilic, hydrogen-oxidizing microaerophiles from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 52: 1349-1359.
17. Gregory LG, Karakas-Sen A, Richardson DJ & Spiro S (2000) Detection of genes for membrane-bound nitrate reductase in nitrate-respiring bacteria and in community DNA. FEMS Microbiol Lett 183: 275-279.
18. Gregory LG, Bond PL, Richardson DJ & Spiro S (2003) Characterization of a nitrate-respiring bacterial community using the nitrate reductase gene (narG) as a functional marker. Microbiology 149: 229-237.
19. 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.
20. Holland SM (2008) Analytic rarefaction. Available at http://www.huntmountainsoftware.com/index.html.
21. Huber JA, Butterfield DA & Baross JA (2003) Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol Ecol 43: 393-409.
22. 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.
23. Inagaki F, Takai K, Nealson KH & Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54: 1477-1482.
24. Karl DM (1995) Ecology of free-living, hydrothermal vent microbial communities. The Microbiology of Deep-sea Hydrothermal Vents (Karl DM, ed.), pp. 35-124. CRC Press, Inc, Boca Raton, FL.
25. Kaye JZ & Baross JA (2000) High incidence of halotolerant bacteria in Pacific hydrothermal-vent and pelagic environments. FEMS Microbiol Ecol 32: 249-260.
26. Kaye JZ, Sylvan JB, Edwards KJ & Baross JA (2011) Halomonas and Marinobacter ecotypes from hydrothermal vent, subseafloor, and deep-sea environments. FEMS Microbiol Ecol 75: 123-133.
27. Longnecker K & Reysenbach A-L (2001) Expansion of the geographic distribution of a novel lieneage of ε-proteobacteria to a hydrothermal vent site on the Southern East Pacific Rise. FEMS Microbiol Ecol 35: 287-293.
28. 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.
29. Madigan MT, Martinko JM & Parker J (2000) Brock Biology of Microorganisms, 07458. Prentice Hall, Upper Saddle River, NJ.
30. Millero FJ (2006) Nitrogen compounds in seawater. Chemical Oceanography (Group TaF, eds), pp. 305-319. CRC Press, Boca Raton, FL.
31. Miroshnichenko ML, L'Haridon S, Schumann P, Spring S, Bonch-Osmolovskaya EA, Jeanthon C & Stackebrandt E (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.
32. Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K & Sako Y (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environ Microbiol 7: 1619-1632.
33. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K & Horikoshi K (2007) Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens. P Natl Acad Sci USA 104: 12146-12150.
34. Nees HA, Moore TS, Mullaugh KM et al. (2008) Hydrothermal vent mussel habitat chemistry, pre- and post-eruption at 9°50′ North on the East Pacific Rise. J Shellfish Res 27: 169-175.
35. 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.
36. Philippot L (2002) Denitifying genes in bacterial and archaealgenomes. Biochem Biophys Acta 1577: 355-376.
37. Philippot L (2005) Tracking nitrate reducers and denitrifiers in the environment. Biochem Soc Trans 33 (Pt 1): 200-204.
38. Potter LC, Millington P, Griffiths L, Thomas GH & Cole J (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.
39. Potter L, Angove H, Richardson D & Cole J (2001) Nitrate reduction in the periplasm of gram-negative bacteria. Adv Microb Physiol 45: 51-112.
40. Robidart JC, Roque A, Song P & Girguis PR (2011) Linking hydrothermal geochemistry to organismal physiology: physiological versatility in Riftia pachyptila from sedimented and basalt-hosted vents. PLoS One 6: e21692.
41. Rowley G, Hensen D, Felgate H et al. (2012) Resolving the contributions of the membrane-bound and periplasmic nitrate reductase systems to nitric oxide and nitrous oxide production in Salmonella enterica serovar Typhimurium. Biochem J 441: 755-762.
42. Schrenk MO, Huber JA & Edwards KJ (2010) Microbial provinces in the subseafloor. Ann Rev Mar Sci 2: 279-304.
43. Shannon CE & Weaver W (1949) The Mathematical Theory of Communication. University of Illinois Press, Urbana.
44. Sievert S & Vetriani C (2012) Chemoautotrophy at deep-sea vents. Past, present and future. Oceanography 25: 218-233.
45. Sikorski J, Munk C, Lapidus A et al. (2010) Complete genome sequence of Sulfurimonas autotrophica type strain (OK10). Stand Genomic Sci 3: 194-202.
46. Smith JL, Campbell BJ, Hanson TE, Zhang CL & Cary SC (2008) Nautilia profundicola sp. nov., a thermophilic, sulfur-reducing epsilonproteobacterium from deep-sea hydrothermal vents. Int J Syst Evol Microbiol 58: 1598-1602.
47. 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.
48. Vetriani C, Jannasch HW, MacGregor BJ, Stahl DA & Reysenbach AL (1999) Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol 65: 4375-4384.
49. 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.
50. Voordeckers JW, 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.
51. 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.
52. Waksman SA, Hotchkiss M & Carey CL (1933) Marine bacteria and their role in the cycle of life in the sea. Biol Bull 65: 146-149.
53. 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.
54. Xie W, Wang F, Guo L et al. (2011) Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries. ISME J 5: 414-426.