Skip to main content
SpringerLink
Log in

Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats

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

Abstract

Ammonia oxidation in marine and terrestrial ecosystems plays a pivotal role in the cycling of nitrogen and carbon. Recent discoveries have shown that ammonia-oxidizing archaea (AOA) are both abundant and diverse in these systems, yet very little is known about their physiology. Here we report a physiological analysis of a novel low-salinity-type AOA enriched from the San Francisco Bay estuary, Candidatus Nitrosoarchaeum limnia strain SFB1. N. limnia has a slower growth rate than Nitrosopumilus maritimus and Nitrososphaera viennensis EN76, the only pure AOA isolates described to date, but the growth rate is comparable to the growth of marine AOA enrichment cultures. The growth rate only slightly decreased when N. limnia was grown under lower-oxygen conditions (5.5 % oxygen in the headspace). Although N. limnia was capable of growth at 75 % of seawater salinity, there was a longer lag time, incomplete oxidation of ammonia to nitrite, and slower overall growth rate. Allylthiourea (ATU) only partially inhibited growth and ammonia oxidation by N. limnia at concentrations known to completely inhibit bacterial ammonia oxidation. Using electron microscopy, we confirmed the presence of flagella as suggested by various flagellar biosynthesis genes in the N. limnia genome. We demonstrate that N. limnia is representative of a low-salinity estuarine AOA ecotype and that more than 85 % of its proteins have highest identity to other coastal and estuarine metagenomic sequences. Our findings further highlight the physiology of N. limnia and help explain its ecological adaptation to low-salinity niches.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Schleper C, Nicol G (2010) Ammonia-oxidising archaea—physiology, ecology and evolution. Adv Microb Physiol 57:1–41

    Article  PubMed  CAS  Google Scholar 

  2. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869. doi:10.1111/j.1574-6976.2009.00179.x

    Article  PubMed  CAS  Google Scholar 

  3. Schleper C (2010) Ammonia oxidation: different niches for bacteria and archaea? ISME J 4:1092–1094. doi:10.1038/ismej.2010.111

    Article  PubMed  Google Scholar 

  4. Martens-Habbena W, Berube PM, Urakawa H, La Torre De JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976–979. doi:10.1038/nature08465

    Article  PubMed  CAS  Google Scholar 

  5. Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR (2011) Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6:e16626

    Article  PubMed  CAS  Google Scholar 

  6. Mosier A (2011) Microbial nitrogen cycling dynamics in coastal systems. Dissertation, Stanford University, Stanford

  7. Stahl D, Amann R, Stackebrandt E, Goodfellow M (1991) Development and application of nucleic acid probes. In: Nucleic acid techniques in bacterial systematics. Wiley, Chichester

    Google Scholar 

  8. Amann RI, Zarda B, Stahl DA, Schleifer KH (1992) Identification of individual prokaryotic cells by using enzyme-labeled, rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 58:3007–3011

    PubMed  CAS  Google Scholar 

  9. Daims H, Brühl A, Amann R, Schleifer KH, 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

    Article  PubMed  CAS  Google Scholar 

  10. Hunt DE et al (2008) Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320:1081–1085. doi:10.1126/science.1157890

    Article  PubMed  CAS  Google Scholar 

  11. Mosier A, Francis C (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002–3016. doi:10.1111/j.1462-2920.2008.01764.x

    Article  PubMed  CAS  Google Scholar 

  12. Seshadri R, Kravitz SA, Smarr L, Gilna P, Frazier M (2007) CAMERA: a community resource for metagenomics. PLoS Biol 5:e75. doi:10.1371/journal.pbio.0050075

    Article  PubMed  Google Scholar 

  13. Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci USA. doi:10.1073/pnas.1107196108

  14. Santoro AE, Casciotti KL (2011) Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J 5:1796–1808. doi:10.1038/ismej.2011.58

    Article  PubMed  CAS  Google Scholar 

  15. de la Torre J, Walker C, Ingalls A, Könneke M, Stahl D (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818. doi:10.1111/j.1462-2920.2007.01506.x

    Article  PubMed  Google Scholar 

  16. Park B-J et al (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  PubMed  CAS  Google Scholar 

  17. Tourna M et al (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci 108:8420–8425. doi:10.1073/pnas.1013488108

    Article  PubMed  CAS  Google Scholar 

  18. Loescher CR et al (2012) Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosci Discuss 9:2095–2122. doi:10.5194/bgd-9-2095-2012

    Article  Google Scholar 

  19. Hatzenpichler R et al (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci 105:2134–2139. doi:10.1073/pnas.0708857105

    Article  PubMed  CAS  Google Scholar 

  20. 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  PubMed  CAS  Google Scholar 

  21. Hooper AB, Terry KR (1973) Specific inhibitors of ammonia oxidation in Nitrosomonas. J Bacteriol 115:480–485

    PubMed  CAS  Google Scholar 

  22. Ginestet P, Audic J, Urbain V, Block J (1998) Estimation of nitrifying bacterial activities by measuring oxygen uptake in the presence of the metabolic inhibitors allylthiourea and azide. Appl Environ Microbiol 64:2266–2268

    PubMed  CAS  Google Scholar 

  23. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125. doi:10.1126/science.1176985

    Article  PubMed  CAS  Google Scholar 

  24. Codispoti LA (2010) Oceans. Interesting times for marine N2O. Science 327:1339–1340. doi:10.1126/science.1184945

    Article  PubMed  CAS  Google Scholar 

  25. Braker G, Conrad R (2011) Diversity, structure, and size of N2O-producing microbial communities in soils—what matters for their functioning? Adv Appl Microbiol 75:33–70. doi:10.1016/B978-0-12-387046-9.00002-5

    Article  PubMed  CAS  Google Scholar 

  26. Arp DJ, Stein LY (2003) Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Crit Rev Biochem Mol Biol 38:471–495. doi:10.1080/10409230390267446

    Article  PubMed  CAS  Google Scholar 

  27. Cantera J, Stein L (2007) Molecular diversity of nitrite reductase genes (nirK) in nitrifying bacteria. Environ Microbiol 9:765–776

    Article  PubMed  Google Scholar 

  28. Treusch A et al (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    Article  PubMed  CAS  Google Scholar 

  29. Yooseph S et al (2007) The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol 5:e16. doi:10.1371/journal.pbio.0050016

    Article  PubMed  Google Scholar 

  30. Bartossek R, Nicol GW, Lanzen A, Klenk H-P, Schleper C (2010) Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context. Environ Microbiol 12:1075–1088. doi:10.1111/j.1462-2920.2010.02153.x

    Article  PubMed  CAS  Google Scholar 

  31. Walker CB et al (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107:8818–8823. doi:10.1073/pnas.0913533107

    Article  PubMed  CAS  Google Scholar 

  32. Lund, M. B., Smith, J. M., & Francis, C. A. (2012). Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea. The ISME Journal. doi:10.1038/ismej.2012.40

  33. Santoro AE, Buchwald C, Mcilvin MR, Casciotti KL (2011) Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333:1282–1285

    Article  PubMed  CAS  Google Scholar 

  34. Dundee L, Hopkins D (2001) Different sensitivities to oxygen of nitrous oxide production by Nitrosomonas europaea and Nitrosolobus multiformis. Soil Biol Biochem 33:1563–1565

    Article  CAS  Google Scholar 

  35. Cantera J, Stein L (2007) Role of nitrite reductase in the ammonia-oxidizing pathway of Nitrosomonas europaea. Arch Microbiol 188:349–354

    Article  PubMed  CAS  Google Scholar 

  36. Hollibaugh JT, Gifford S, Sharma S, Bano N, Moran MA (2011) Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage. ISME J 5:866–878. doi:10.1038/ismej.2010.172

    Article  PubMed  CAS  Google Scholar 

  37. Hunter S et al (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211–5. doi:10.1093/nar/gkn785

    Article  PubMed  CAS  Google Scholar 

  38. Könneke M et al (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  39. Wanner BL (1993) Gene regulation by phosphate in enteric bacteria. J Cell Biochem 51:47–54. doi:10.1002/jcb.240510110

    Article  PubMed  CAS  Google Scholar 

  40. Oganesyan V et al (2005) Crystal structure of the “PhoU-like” phosphate uptake regulator from Aquifex aeolicus. J Bacteriol 187:4238

    Article  PubMed  CAS  Google Scholar 

  41. Gebhard S, Ekanayaka N, Cook GM (2009) The low-affinity phosphate transporter PitA is dispensable for in vitro growth of Mycobacterium smegmatis. BMC Microbiol 9:254. doi:10.1186/1471-2180-9-254

    Article  PubMed  Google Scholar 

  42. Wankel S, Kendall C, Francis C, Paytan A (2006) Nitrogen sources and cycling in the San Francisco Bay estuary: a nitrate dual isotopic composition approach. Limnol Oceanogr 51:1654–1664

    Article  CAS  Google Scholar 

  43. Peterson D et al (1985) Interannual variability in dissolved inorganic nutrients in Northern San Francisco Bay estuary. Hydrobiologia 129:37–58

    Article  CAS  Google Scholar 

  44. Jassby A (2008) Phytoplankton in the Upper San Francisco estuary: recent biomass trends, their causes and their trophic significance. San Francisco Estuary Watershed Sci 6:1–24

    Google Scholar 

  45. Balch W, Fox G, Magrum L, Woese C, Wolfe R (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296

    PubMed  CAS  Google Scholar 

  46. Biebl H, Pfennig N (1978) Growth yields of green sulfur bacteria in mixed cultures with sulfur and sulfate reducing bacteria. Arch Microbiol 117:9–16

    Article  CAS  Google Scholar 

  47. Pernthaler A, Pernthaler J (2007) Fluorescence in situ hybridization for the identification of environmental microbes. Methods Mol Biol 353:153–164

    PubMed  Google Scholar 

Download references

Acknowledgments

We thank L.M. Joubert at the Stanford Cell Sciences Imaging Facility for performing electron microscopy. This work was funded by a National Science Foundation grant (OCE-0847266) to C.A.F. and by the Diversifying Academia, Recruiting Excellence DARE Doctoral Fellowship (Stanford University) and the Environmental Protection Agency STAR Graduate Fellowship to A.C.M.

Author information

Author notes

  1. Annika C. Mosier

    Present address: University of California, Berkeley, CA, 94720, USA

Authors and Affiliations

  1. Department of Environmental Earth System Science, Stanford University, Stanford, CA, 94305-4216, USA

    Annika C. Mosier, Marie B. Lund & Christopher A. Francis

Authors
  1. Annika C. Mosier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie B. Lund
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher A. Francis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Annika C. Mosier.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 31 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mosier, A.C., Lund, M.B. & Francis, C.A. Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats. Microb Ecol 64, 955–963 (2012). https://doi.org/10.1007/s00248-012-0075-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0075-1

Keywords

Search

Navigation