Skip to main content

Advertisement

Log in

Detection and Diversity of the Nitrite Oxidoreductase Alpha Subunit (nxrA) Gene of Nitrospina in Marine Sediments

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Nitrite-oxidizing bacteria (NOB) are chemolithoautotrophs that catalyze the oxidation of nitrite to nitrate, which is the second step of aerobic nitrification. In marine ecosystems, Nitrospina is assumed to be a major contributor to nitrification. To date, two strains of Nitrospina have been isolated from marine environments. Despite their ecological relevance, their ecophysiology and environmental distribution are understudied owing to fastidious cultivation techniques and the lack of a sufficient functional gene marker. To estimate the abundance, diversity, and distribution of Nitrospina in various marine sediments, we used nxrA, which encodes the alpha subunit of nitrite oxidoreductase, as a functional and phylogenetic marker. We observed that Nitrospina diversity in polar sediments was significantly lower than that of non-polar samples. Moreover, nxrA-like sequences revealed an unexpected diversity of Nitrospina, with approximately 41,000 different sequences based on a 95% similarity cutoff from six marine sediments. We detected nxrA gene copy numbers of up to 3.57 × 104 per gram of marine sediment sample. The results of this study provide insight into the distribution and diversity of Nitrospina, which is fundamentally important for understanding their contribution to the nitrogen cycle in marine sediments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Jetten MS, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen UG, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MC, Kuenen JG (1998) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22:421–437

    Article  CAS  PubMed  Google Scholar 

  2. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688. doi:10.1073/pnas.0506625102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809. doi:10.1038/nature04983

    Article  CAS  PubMed  Google Scholar 

  6. Park SJ, Park BJ, Rhee SK (2008) Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 12:605–615. doi:10.1007/s00792-008-0165-7

    Article  CAS  PubMed  Google Scholar 

  7. Junier P, Molina V, Dorador C, Hadas O, Kim OS, Junier T, Witzel JP, Imhoff JF (2010) Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment. Appl Microbiol Biotechnol 85:425–440. doi:10.1007/s00253-009-2228-9

    Article  CAS  PubMed  Google Scholar 

  8. Ish-Am O, Kristensen DM, Ruppin E (2015) Evolutionary conservation of bacterial essential metabolic genes across all bacterial culture media. PLoS ONE 10:e0123785. doi:10.1371/journal.pone.0123785

    Article  PubMed  PubMed Central  Google Scholar 

  9. Eisen JA (1995) The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol 41:1105–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC, Huang Z, Wu W, Gu B, Jardine P, Criddle C, Zhou J (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J 1:67–77. doi:10.1038/ismej.2007.2

    Article  CAS  PubMed  Google Scholar 

  11. Case RJ, Boucher Y, Dahllöf I, Holmström C, Doolittle WF, Kjelleberg S (2007) Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microbiol 73:278–288. doi:10.1128/AEM.01177-06

    Article  CAS  PubMed  Google Scholar 

  12. Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23:563–590

    Article  CAS  PubMed  Google Scholar 

  13. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570. doi:10.1038/nature12375

    Article  CAS  PubMed  Google Scholar 

  14. Spieck E, Bock E (2005) The lithoautotrophic nitrite-oxidizing bacteria. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s Manual® of systematic bacteriology: volume two: the Proteobacteria, part A Introductory essays. Springer US, Boston, pp 149–153

    Chapter  Google Scholar 

  15. Garrity GM, Holt JG, Spieck E, Bock E, Johnson DB, Spring S, Schleifer K-H, Maki JS (2001) Phylum BVIII. Nitrospirae phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s Manual® of systematic bacteriology: volume one: the Archaea and the deeply branching and phototrophic bacteria. Springer New York, New York, pp 451–464

    Google Scholar 

  16. Sorokin DY, Lucker S, Vejmelkova D, Kostrikina NA, Kleerebezem R, Rijpstra WI, Damste JS, Le Paslier D, Muyzer G, Wagner M, van Loosdrecht MC, Daims H (2012) Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J 6:2245–2256. doi:10.1038/ismej.2012.70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yamanaka T, Fukumori Y (1988) The nitrite oxidizing system of Nitrobacter winogradskyi. FEMS Microbiol Rev 4:259–270

    Article  CAS  PubMed  Google Scholar 

  18. Watson SW, Waterbury JB Characteristics of two marine nitrite oxidizing bacteria, Nitrospina gracilis nov. gen. nov. sp. and Nitrococcus mobilis nov. gen. nov. sp. Arch Mikrobiol 77:203–230. doi: 10.1007/bf00408114

  19. van Kessel MA, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJ, Kartal B, Jetten MS, Lucker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559. doi:10.1038/nature16459

    PubMed  PubMed Central  Google Scholar 

  20. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509. doi:10.1038/nature16461

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Koch H, Galushko A, Albertsen M, Schintlmeister A, Gruber-Dorninger C, Lucker S, Pelletier E, Le Paslier D, Spieck E, Richter A, Nielsen PH, Wagner M, Daims H (2014) Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345:1052–1054. doi:10.1126/science.1256985

    Article  CAS  PubMed  Google Scholar 

  22. Haaijer SC, Ji K, van Niftrik L, Hoischen A, Speth D, Jetten MS, Damste JS, Op den Camp HJ (2013) A novel marine nitrite-oxidizing Nitrospira species from Dutch coastal North Sea water. Front Microbiol 4:60. doi:10.3389/fmicb.2013.00060

    Article  PubMed  PubMed Central  Google Scholar 

  23. Spieck E, Keuter S, Wenzel T, Bock E, Ludwig W (2014) Characterization of a new marine nitrite oxidizing bacterium, Nitrospina watsonii sp. nov., a member of the newly proposed phylum “Nitrospinae”. Syst Appl Microbiol 37:170–176. doi:10.1016/j.syapm.2013.12.005

    Article  CAS  PubMed  Google Scholar 

  24. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9:1162–1175. doi:10.1111/j.1462-2920.2007.01239.x

    Article  CAS  PubMed  Google Scholar 

  25. Santoro AE, Casciotti KL, Francis CA (2010) Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ Microbiol 12:1989–2006. doi:10.1111/j.1462-2920.2010.02205.x

    Article  CAS  PubMed  Google Scholar 

  26. Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damste JS, Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76:7575–7587. doi:10.1128/AEM.01478-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Beman JM, Leilei Shih J, Popp BN (2013) Nitrite oxidation in the upper water column and oxygen minimum zone of the eastern tropical North Pacific Ocean. ISME J 7:2192–2205. doi:10.1038/ismej.2013.96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lüke C, Speth DR, Kox MA, Villanueva L, Jetten MS (2016) Metagenomic analysis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone. PeerJ 4:e1924. doi:10.7717/peerj.1924

    Article  PubMed  PubMed Central  Google Scholar 

  29. Lücker S, Nowka B, Rattei T, Spieck E, Daims H (2013) The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front Microbiol 4:27. doi:10.3389/fmicb.2013.00027

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ngugi DK, Blom J, Stepanauskas R, Stingl U (2016) Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines. ISME J 10:1383–1399. doi:10.1038/ismej.2015.214

    Article  CAS  PubMed  Google Scholar 

  31. Levipan HA, Molina V, Fernandez C (2014) Nitrospina-like bacteria are the main drivers of nitrite oxidation in the seasonal upwelling area of the Eastern South Pacific (Central Chile approximately 36 degrees S). Environ Microbiol Rep 6:565–573

    Article  CAS  PubMed  Google Scholar 

  32. Regan JM, Harrington GW, Baribeau H, De Leon R, Noguera DR (2003) Diversity of nitrifying bacteria in full-scale chloraminated distribution systems. Water Res 37:197–205

    Article  CAS  PubMed  Google Scholar 

  33. Poly F, Wertz S, Brothier E, Degrange V (2008) First exploration of Nitrobacter diversity in soils by a PCR cloning-sequencing approach targeting functional gene nxrA. FEMS Microbiol Ecol 63:132–140. doi:10.1111/j.1574-6941.2007.00404.x

    Article  CAS  PubMed  Google Scholar 

  34. Vanparys B, Spieck E, Heylen K, Wittebolle L, Geets J, Boon N, De Vos P (2007) The phylogeny of the genus Nitrobacter based on comparative rep-PCR, 16S rRNA and nitrite oxidoreductase gene sequence analysis. Syst Appl Microbiol 30:297–308. doi:10.1016/j.syapm.2006.11.006

    Article  CAS  PubMed  Google Scholar 

  35. Wertz S, Poly F, Le Roux X, Degrange V (2008) Development and application of a PCR-denaturing gradient gel electrophoresis tool to study the diversity of Nitrobacter-like nxrA sequences in soil. FEMS Microbiol Ecol 63:261–271. doi:10.1111/j.1574-6941.2007.00416.x

    Article  CAS  PubMed  Google Scholar 

  36. Pester M, Maixner F, Berry D, Rattei T, Koch H, Lucker S, Nowka B, Richter A, Spieck E, Lebedeva E, Loy A, Wagner M, Daims H (2014) NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol 16:3055–3071. doi:10.1111/1462-2920.12300

    Article  CAS  PubMed  Google Scholar 

  37. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310. doi:10.1371/journal.pone.0027310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:10.2307/2408678

    Article  Google Scholar 

  40. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160. doi:10.1111/j.1574-6941.2007.00375.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Park SJ, Park BJ, Jung MY, Kim SJ, Chae JC, Roh Y, Forwick M, Yoon HI, Rhee SK (2011) Influence of deglaciation on microbial communities in marine sediments off the coast of Svalbard, Arctic Circle. Microb Ecol 62:537–548. doi:10.1007/s00248-011-9860-5

    Article  PubMed  Google Scholar 

  42. Jongman RHG, ter Braak CJF, OFR VT (1995) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  43. Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18:50–60

    Article  Google Scholar 

  44. Füssel J, Lam P, Lavik G, Jensen MM, Holtappels M, Gunter M, Kuypers MM (2012) Nitrite oxidation in the Namibian oxygen minimum zone. ISME J 6:1200–1209. doi:10.1038/ismej.2011.178

    Article  PubMed  Google Scholar 

  45. Choi H, Koh HW, Kim H, Chae JC, Park SJ (2016) Microbial community composition in the marine sediments of Jeju Island: next-generation sequencing surveys. J Microbiol Biotechnol 26:883–890. doi:10.4014/jmb.1512.12036

    Article  PubMed  Google Scholar 

  46. Mao DP, Zhou Q, Chen CY, Quan ZX (2012) Coverage evaluation of universal bacterial primers using the metagenomic datasets. BMC Microbiol 12:66. doi:10.1186/1471-2180-12-66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Poretsky R, Rodriguez RL, Luo C, Tsementzi D, Konstantinidis KT (2014) Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS One 9:e93827. doi:10.1371/journal.pone.0093827

    Article  PubMed  PubMed Central  Google Scholar 

  48. Boucher Y, Douady CJ, Papke RT, Walsh DA, Boudreau ME, Nesbo CL, Case RJ, Doolittle WF (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet 37:283–328. doi:10.1146/annurev.genet.37.050503.084247

    Article  CAS  PubMed  Google Scholar 

  49. Attard E, Poly F, Commeaux C, Laurent F, Terada A, Smets BF, Recous S, Roux XL (2010) Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environ Microbiol 12:315–326. doi:10.1111/j.1462-2920.2009.02070.x

    Article  CAS  PubMed  Google Scholar 

  50. 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. doi:10.1099/mic.0.25849-0

    Article  CAS  PubMed  Google Scholar 

  51. Junge K, Eicken H, Deming JW (2004) Bacterial activity at −2 to −20 degrees C in Arctic wintertime sea ice. Appl Environ Microbiol 70:550–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Alonso-Sáez L, Galand PE, Casamayor EO, Pedrós-Alió C, Bertilsson S (2010) High bicarbonate assimilation in the dark by Arctic bacteria. ISME J 4:1581–1590. doi:10.1038/ismej.2010.69

    Article  PubMed  Google Scholar 

  53. Alawi M, Lipski A, Sanders T, Pfeiffer EM, Spieck E (2007) Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium from the Siberian Arctic. ISME J 1:256–264

    Article  CAS  PubMed  Google Scholar 

  54. Alawi M, Off S, Kaya M, Spieck E (2009) Temperature influences the population structure of nitrite-oxidizing bacteria in activated sludge. Environ Microbiol Rep 1:184–190. doi:10.1111/j.1758-2229.2009.00029.x

    Article  CAS  PubMed  Google Scholar 

  55. Christner BC, Priscu JC, Achberger AM, Barbante C, Carter SP, Christianson K, Michaud AB, Mikucki JA, Mitchell AC, Skidmore ML, Vick-Majors TJ, Team WS (2014) A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512:310–313. doi:10.1038/nature13667

    Article  CAS  PubMed  Google Scholar 

  56. Kim JG, Park SJ, Quan ZX, Jung MY, Cha IT, Kim SJ, Kim KH, Yang EJ, Kim YN, Lee SH, Rhee SK (2014) Unveiling abundance and distribution of planktonic Bacteria and Archaea in a polynya in Amundsen Sea, Antarctica. Environ Microbiol 16:1566–1578. doi:10.1111/1462-2920.12287

    Article  PubMed  Google Scholar 

  57. Sun MY, Dafforn KA, Johnston EL, Brown MV (2013) Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. Environ Microbiol 15:2517–2531. doi:10.1111/1462-2920.12133

    Article  PubMed  Google Scholar 

  58. Hernández DL, Hobbie SE (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335:397–411. doi:10.1007/s11104-010-0428-9

    Article  Google Scholar 

  59. Gillan DC, Danis B, Pernet P, Joly G, Dubois P (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Environ Microbiol 71:679–690. doi:10.1128/AEM.71.2.679-690.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Koch H, Lucker S, Albertsen M, Kitzinger K, Herbold C, Spieck E, Nielsen PH, Wagner M, Daims H (2015) Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc Natl Acad Sci U S A 112:11371–11376. doi:10.1073/pnas.1506533112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Daims H, Maixner F, Lucker S, Stoecker K, Hace K, Wagner M (2006) Ecophysiology and niche differentiation of Nitrospira-like bacteria, the key nitrite oxidizers in wastewater treatment plants. Water Sci Technol 54:21–27

    Article  CAS  PubMed  Google Scholar 

  62. Maixner F, Noguera DR, Anneser B, Stoecker K, Wegl G, Wagner M, Daims H (2006) Nitrite concentration influences the population structure of Nitrospira-like bacteria. Environ Microbiol 8:1487–1495. doi:10.1111/j.1462-2920.2006.01033.x

    Article  CAS  PubMed  Google Scholar 

  63. Gruber-Dorninger C, Pester M, Kitzinger K, Savio DF, Loy A, Rattei T, Wagner M, Daims H (2015) Functionally relevant diversity of closely related Nitrospira in activated sludge. ISME J 9:643–655. doi:10.1038/ismej.2014.156

    Article  CAS  PubMed  Google Scholar 

  64. Fujitani H, Aoi Y, Tsuneda S (2013) Selective enrichment of two different types of Nitrospira-like nitrite-oxidizing bacteria from a wastewater treatment plant. Microbes Environ 28:236–243

    Article  PubMed  PubMed Central  Google Scholar 

  65. Starkenburg SR, Chain PS, Sayavedra-Soto LA, Hauser L, Land ML, Larimer FW, Malfatti SA, Klotz MG, Bottomley PJ, Arp DJ, Hickey WJ (2006) Genome sequence of the chemolithoautotrophic nitrite-oxidizing bacterium Nitrobacter winogradskyi Nb-255. Appl Environ Microbiol 72:2050–2063. doi:10.1128/AEM.72.3.2050-2063.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Damste JS, Spieck E, Le Paslier D, Daims H (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci U S A 107:13479–13484. doi:10.1073/pnas.1003860107

    Article  PubMed  PubMed Central  Google Scholar 

  67. Grein F, Ramos AR, Venceslau SS, Pereira IA (2013) Unifying concepts in anaerobic respiration: insights from dissimilatory sulfur metabolism. Biochim Biophys Acta 1827:145–160. doi:10.1016/j.bbabio.2012.09.001

    Article  CAS  PubMed  Google Scholar 

  68. Muller JA, DasSarma S (2005) Genomic analysis of anaerobic respiration in the archaeon Halobacterium sp. strain NRC-1: dimethyl sulfoxide and trimethylamine N-oxide as terminal electron acceptors. J Bacteriol 187:1659–1667. doi:10.1128/JB.187.5.1659-1667.2005

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (no. 2015R1C1A1A01053750) and the C1 Gas Refinery Program through the NRF funded by the Ministry of Science, ICT & Future Planning (no. 2015M3D3A1A01064881). We thank the editor and two anonymous reviewers for their constructive and scientific comments, which helped us to improve the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hirotsugu Fujitani or Soo-Je Park.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 751 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rani, S., Koh, HW., Rhee, SK. et al. Detection and Diversity of the Nitrite Oxidoreductase Alpha Subunit (nxrA) Gene of Nitrospina in Marine Sediments. Microb Ecol 73, 111–122 (2017). https://doi.org/10.1007/s00248-016-0897-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0897-3

Keywords

Navigation