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Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea

  • Environmental Microbiology
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Abstract

Despite the explosion of metagenomic sequencing data, using -omics data to predict environmental biogeochemistry remains a challenge. One or a few genes (referred to as marker genes) in a metabolic pathway of interest in meta-omic data are typically used to represent the prevalence of a biogeochemical reaction. This approach often fails to demonstrate a consistent relationship between gene abundance and an ecosystem process rate. One reason this may occur is if a marker gene is not a good representative of a complete pathway. Here, we map the presence of 11 nitrogen (N)-cycling pathways in over 6000 complete bacterial and archaeal genomes using the Integrated Microbial Genomes database. Incomplete N-cycling pathways occurred in 39% of surveyed archaeal and bacterial species revealing a weakness in current marker-gene analyses. Furthermore, we found that most organisms have limited ability to utilize inorganic N in multiple oxidation states. This suggests that inter-organism exchange of inorganic N compounds is common, highlighting the importance of both community composition and spatial structure in determining the extent of recycling versus loss in an ecosystem.

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References

  1. Di HJ, Cameron KC, Podolyan A, Robinson A (2014) Effect of soil moisture status and a nitrification inhibitor, dicyandiamide, on ammonia oxidizer and denitrifier growth and nitrous oxide emissions in a grassland soil. Soil Biol. Biochem. 73:59–68. https://doi.org/10.1016/j.soilbio.2014.02.011

    Article  CAS  Google Scholar 

  2. Morales SE, Jha N, Saggar S (2015) Biogeography and biophysicochemical traits link N2O emissions, N2O emission potential and microbial communities across New Zealand pasture soils. Soil Biol. Biochem. 82:87–98. https://doi.org/10.1016/j.soilbio.2014.12.018

    Article  CAS  Google Scholar 

  3. Rocca JD, Hall EK, Lennon JT, Evans SE, Waldrop MP, Cotner JB, Nemergut DR, Graham EB, Wallenstein MD (2015) Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed. Isme J 9:1693–1699. https://doi.org/10.1038/ismej.2014.252

    Article  PubMed  CAS  Google Scholar 

  4. Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics 13:162. https://doi.org/10.1186/1471-2164-13-162

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  5. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5:539–554. https://doi.org/10.1046/j.1462-2920.2003.00451.x

    Article  PubMed  CAS  Google Scholar 

  6. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol. Biol. Evol. 21:541–554. https://doi.org/10.1093/molbev.msh047

    Article  PubMed  CAS  Google Scholar 

  7. Nelson MB, Berlemont R, Martiny AC, Martiny JBH (2015) Nitrogen cycling potential of a grassland litter microbial community. Appl Environ Microbiol 81:7012–7022. https://doi.org/10.1128/Aem.02222-15

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  8. Nelson MB, Martiny AC, Martiny JBH (2016) Global biogeography of microbial nitrogen-cycling traits in soil. Proc Natl Acad Sci USA 113:8033–8040. https://doi.org/10.1073/pnas.1601070113

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  9. Brady A, Salzberg S (2011) PhymmBL expanded: confidence scores, custom databases, parallelization and more. Nat Methods 8:367–367. https://doi.org/10.1038/nmeth0511-367

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The ribosomal database project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 33:D294–D296. https://doi.org/10.1093/nar/gki038

    Article  PubMed  CAS  Google Scholar 

  11. Mason OU, Scott NM, Gonzalez A, Robbins-Pianka A, Baelum J, Kimbrel J, Bouskill NJ, Prestat E, Borglin S, Joyner DC, Fortney JL, Jurelevicius D, Stringfellow WT, Alvarez-Cohen L, Hazen TC, Knight R, Gilbert JA, Jansson JK (2014) Metagenomics reveals sediment microbial community response to Deepwater horizon oil spill. ISME J 8:1464–1475. https://doi.org/10.1038/ismej.2013.254

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  12. Morales SE, Cosart T, Holben WE (2010) Bacterial gene abundances as indicators of greenhouse gas emission in soils. ISME J 4:799–808. https://doi.org/10.1038/ismej.2010.8

    Article  PubMed  CAS  Google Scholar 

  13. Tu QC, He ZL, Wu LY, Xue K, Xie G, Chain P, Reich PB, Hobbie SE, Zhou JZ (2017) Metagenomic reconstruction of nitrogen cycling pathways in a CO2- enriched grassland ecosystem. Soil Biol. Biochem. 106:99–108. https://doi.org/10.1016/j.soilbio.2016.12.017

    Article  CAS  Google Scholar 

  14. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. https://doi.org/10.1126/science.1136674

    Article  PubMed  CAS  Google Scholar 

  15. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman D (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. https://doi.org/10.2307/2269431

    Article  Google Scholar 

  16. Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms - a review. Soil Biol. Biochem. 42:2058–2067. https://doi.org/10.1016/j.soilbio.2010.08.021

    Article  CAS  Google Scholar 

  17. Zehr JP, Ward BB (2002) Nitrogen cycling in the ocean: new perspectives on processes and paradigms. Appl Environ Microbiol 68:1015–1024. https://doi.org/10.1128/Aem.68.3.1015-1024.2002

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Isobe K, Ohte N (2014) Ecological perspectives on microbes involved in N-cycling. Microbes Environ. 29:4–16. https://doi.org/10.1264/jsme2.ME13159

    Article  PubMed  PubMed Central  Google Scholar 

  19. Berlemont R, Martiny AC (2015) Genomic potential for polysaccharide deconstruction in Bacteria. Appl Environ Microbiol 81:1513–1519. https://doi.org/10.1128/Aem.03718-14

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44:D457–D462. https://doi.org/10.1093/nar/gkv1070

    Article  PubMed  CAS  Google Scholar 

  21. Markowitz VM, Chen IMA, Palaniappan K, Chu K, Szeto E, Pillay M, Ratner A, Huang JH, Woyke T, Huntemann M, Anderson I, Billis K, Varghese N, Mavromatis K, Pati A, Ivanova NN, Kyrpides NC (2014) IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 42:D560–D567. https://doi.org/10.1093/nar/gkt963

    Article  PubMed  CAS  Google Scholar 

  22. Carlson CA, Ingraham JL (1983) Comparison of denitrification by Pseudomonas-Stutzeri, Pseudomonas-aeruginosa, and Paracoccus-Denitrificans. Appl Environ Microbiol 45:1247–1253

    PubMed  CAS  PubMed Central  Google Scholar 

  23. Ye RW, Thomas SM (2001) Microbial nitrogen cycles: physiology, genomics and applications. Curr. Opin. Microbiol. 4:307–312

    Article  PubMed  CAS  Google Scholar 

  24. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44:W242–W245. https://doi.org/10.1093/nar/gkw290

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. Amon J, Titgemeyer F, Burkovski A (2010) Common patterns - unique features: nitrogen metabolism and regulation in gram-positive bacteria. FEMS Microbiol. Rev. 34:588–605. https://doi.org/10.1111/j.1574-6976.2010.00216.x

    Article  PubMed  CAS  Google Scholar 

  26. Eisenlord SD, Zak DR (2010) Simulated atmospheric nitrogen deposition alters Actinobacterial community composition in Forest soils. Soil Sci. Soc. Am. J. 74:1157–1166. https://doi.org/10.2136/sssaj2009.0240

    Article  CAS  Google Scholar 

  27. Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol. Lett. 11:1111–1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x

    Article  PubMed  Google Scholar 

  28. Price MN, Dehal PS, Arkin AP (2008) Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol. 9:R4. https://doi.org/10.1186/gb-2008-9-1-r4

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Boto L (2010) Horizontal gene transfer in evolution: facts and challenges. Proc. Biol. Sci. 277:819–827. https://doi.org/10.1098/rspb.2009.1679

    Article  PubMed  Google Scholar 

  30. Eberl L, Ammendola A, Rothballer MH, Givskov M, Sternberg C, Kilstrup M, Schleifer KH, Molin S (2000) Inactivation of gltB abolishes expression of the assimilatory nitrate reductase gene (nasB) in Pseudomonas putida KT2442. J Bacteriol 182:3368–3376. https://doi.org/10.1128/Jb.182.12.3368-3376.2000

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Popescu L, Yona G (2005) Automation of gene assignments to metabolic pathways using high-throughput expression data. BMC Bioinformatics 6:217. https://doi.org/10.1186/1471-2105-6-217

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  32. Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M (2000) Nitric oxide reductases in bacteria. BBA-Bioenergetics 1459:266–273. https://doi.org/10.1016/S0005-2728(00)00161-4

    Article  PubMed  CAS  Google Scholar 

  33. de Vries S, Schroder I (2002) Comparison between the nitric oxide reductase family and its aerobic relatives, the cytochrome oxidases. Biochem. Soc. Trans. 30:662–667. https://doi.org/10.1042/BST0300662

    Article  PubMed  Google Scholar 

  34. Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, Prill RJ, Tripathi A, Gibbons SM, Ackermann G, Navas-Molina JA, Janssen S, Kopylova E, Vazquez-Baeza Y, Gonzalez A, Morton JT, Mirarab S, Zech Xu Z, Jiang L, Haroon MF, Kanbar J, Zhu Q, Jin Song S, Kosciolek T, Bokulich NA, Lefler J, Brislawn CJ, Humphrey G, Owens SM, Hampton-Marcell J, Berg-Lyons D, McKenzie V, Fierer N, Fuhrman JA, Clauset A, Stevens RL, Shade A, Pollard KS, Goodwin KD, Jansson JK, Gilbert JA, Knight R, Earth Microbiome Project C (2017) A communal catalogue reveals Earth's multiscale microbial diversity. Nature 551:457–463. https://doi.org/10.1038/nature24621

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814-+. https://doi.org/10.1038/nbt.2676

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  36. Asshauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31:2882–2884. https://doi.org/10.1093/bioinformatics/btv287

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  37. Hartman WH, Ye RZ, Horwath WR, Tringe SG (2017) A genomic perspective on stoichiometric regulation of soil carbon cycling. Isme J 11:2652–2665. https://doi.org/10.1038/ismej.2017.115

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  38. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546. https://doi.org/10.1038/nature03911

    Article  PubMed  CAS  Google Scholar 

  39. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-Garcia C, Rodriguez G, Massol-Deya A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Loffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc. Natl. Acad. Sci. U. S. A. 109:19709–19714. https://doi.org/10.1073/pnas.1211238109

    Article  PubMed  PubMed Central  Google Scholar 

  40. 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. https://doi.org/10.1038/nature16459

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  41. Cardenas E, Kranabetter JM, Hope G, Maas KR, Hallam S, Mohn WW (2015) Forest harvesting reduces the soil metagenomic potential for biomass decomposition. ISME J 9:2465–2476. https://doi.org/10.1038/ismej.2015.57

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  42. Smith CR, Blair PL, Boyd C, Cody B, Hazel A, Hedrick A, Kathuria H, Khurana P, Kramer B, Muterspaw K, Peck C, Sells E, Skinner J, Tegeler C, Wolfe Z (2016) Microbial community responses to soil tillage and crop rotation in a corn/soybean agroecosystem. Ecol Evol 6:8075–8084. https://doi.org/10.1002/ece3.2553

    Article  PubMed  PubMed Central  Google Scholar 

  43. Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, Thomas BC, Singh A, Wilkins MJ, Karaoz U, Brodie EL, Williams KH, Hubbard SS, Banfield JF (2016) Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun 7. https://doi.org/10.1038/ncomms13219

  44. Embree M, Liu JK, Al-Bassam MM, Zengler K (2015) Networks of energetic and metabolic interactions define dynamics in microbial communities. Proc Natl Acad Sci USA 112:15450–15455. https://doi.org/10.1073/pnas.1506034112

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  45. Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR (2015) Metabolic dependencies drive species co-occurrence in diverse microbial communities (vol 112, pg 6449, 2015). Proc Natl Acad Sci USA 112:E7156–E7156. https://doi.org/10.1073/pnas.1522642113

    Article  CAS  Google Scholar 

  46. Chase AB, Karaoz U, Brodie EL, Gomez-Lunar Z, Martiny AC, Martiny JBH (2017) Microdiversity of an abundant terrestrial bacterium encompasses extensive variation in ecologically relevant traits. Mbio 8. https://doi.org/10.1128/mBio.01809-17

  47. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K, Suzuki Y, Dudek N, Relman DA, Finstad KM, Amundson R, Thomas BC, Banfield JF (2016) A new view of the tree of life. Nat Microbiol 1. https://doi.org/10.1038/Nmicrobiol.2016.48

  48. Koonin EV, Aravind L, Kondrashov AS (2000) The impact of comparative genomics on our understanding of evolution. Cell 101:573–576

    Article  PubMed  CAS  Google Scholar 

  49. Bardgett RD, Streeter TC, Bol R (2003) Soil microbes compete effectively with plants for organic-nitrogen inputs to temperate grasslands. Ecology 84:1277–1287. https://doi.org/10.1890/0012-9658(2003)084[1277:Smcewp]2.0.Co;2

  50. Schulten HR, Schnitzer M (1997) The chemistry of soil organic nitrogen: a review. Biol Fertil Soils 26:1–15. https://doi.org/10.1007/s003740050335

    Article  Google Scholar 

  51. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. https://doi.org/10.1890/03-8002

    Article  Google Scholar 

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Acknowledgements

We thank Cheryl Kuske and Renee Johansen for comments on previous versions of this manuscript.

Funding

This work was supported by the U.S. Department of Energy, Office of Science, Biological and Environmental Research Division, under award number F260LANL2018, and by an Office of Science Graduate Student Research (SCGSR) Fellowship to MA.

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Correspondence to Michaeline B. N. Albright or John Dunbar.

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Albright, M.B.N., Timalsina, B., Martiny, J.B.H. et al. Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea. Microb Ecol 77, 597–606 (2019). https://doi.org/10.1007/s00248-018-1239-4

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