Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea
Abstract
Despite the explosion of metagenomic sequencing data, using -omics data to indicate 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 normally used to represent the prevalence of a biogeochemical reaction. This method 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. Moreover, 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.
- Authors:
-
[1];
[1]
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Mississippi State Univ., Starkville, MS (United States)
- Univ. of California, Irvine, CA (United States)
- Publication Date:
- Research Org.:
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1558043
- Report Number(s):
- LA-UR-18-21897
Journal ID: ISSN 0095-3628
- Grant/Contract Number:
- 89233218CNA000001; F260LANL2018
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbial Ecology
- Additional Journal Information:
- Journal Volume: 77; Journal Issue: 3; Journal ID: ISSN 0095-3628
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Nitrogen cycle; Comparative genomics; Bacteria Archaea
Citation Formats
Albright, Michaeline B. N., Timalsina, Bibek, Martiny, Jennifer B. H., and Dunbar, John. Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea. United States: N. p., 2018.
Web. doi:10.1007/s00248-018-1239-4.
Albright, Michaeline B. N., Timalsina, Bibek, Martiny, Jennifer B. H., & Dunbar, John. Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea. United States. doi:https://doi.org/10.1007/s00248-018-1239-4
Albright, Michaeline B. N., Timalsina, Bibek, Martiny, Jennifer B. H., and Dunbar, John. Mon .
"Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea". United States. doi:https://doi.org/10.1007/s00248-018-1239-4. https://www.osti.gov/servlets/purl/1558043.
@article{osti_1558043,
title = {Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea},
author = {Albright, Michaeline B. N. and Timalsina, Bibek and Martiny, Jennifer B. H. and Dunbar, John},
abstractNote = {Despite the explosion of metagenomic sequencing data, using -omics data to indicate 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 normally used to represent the prevalence of a biogeochemical reaction. This method 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. Moreover, 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.},
doi = {10.1007/s00248-018-1239-4},
journal = {Microbial Ecology},
number = 3,
volume = 77,
place = {United States},
year = {2018},
month = {8}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 6 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Common patterns – unique features: nitrogen metabolism and regulation in Gram-positive bacteria
journal, July 2010
- Amon, Johannes; Titgemeyer, Fritz; Burkovski, Andreas
- FEMS Microbiology Reviews, Vol. 34, Issue 4
Networks of energetic and metabolic interactions define dynamics in microbial communities
journal, November 2015
- Embree, Mallory; Liu, Joanne K.; Al-Bassam, Mahmoud M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 50
Technical Report: Human Alteration of the Global Nitrogen Cycle: Sources and Consequences
journal, August 1997
- Vitousek, Peter M.; Aber, John D.; Howarth, Robert W.
- Ecological Applications, Vol. 7, Issue 3
Nitrogen Cycling Potential of a Grassland Litter Microbial Community
journal, July 2015
- Nelson, Michaeline B.; Berlemont, Renaud; Martiny, Adam C.
- Applied and Environmental Microbiology, Vol. 81, Issue 20
Microbial nitrogen cycles: physiology, genomics and applications
journal, June 2001
- Ye, Rick W.; Thomas, Stuart M.
- Current Opinion in Microbiology, Vol. 4, Issue 3
Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies
journal, October 2008
- Treseder, Kathleen K.
- Ecology Letters, Vol. 11, Issue 10
The Impact of Comparative Genomics on Our Understanding of Evolution
journal, June 2000
- Koonin, Eugene V.; Aravind, L.; Kondrashov, Alexey S.
- Cell, Vol. 101, Issue 6
PhymmBL expanded: confidence scores, custom databases, parallelization and more
journal, April 2011
- Brady, Arthur; Salzberg, Steven
- Nature Methods, Vol. 8, Issue 5
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013
- Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
- Nature Biotechnology, Vol. 31, Issue 9
Pathways of nitrogen utilization by soil microorganisms – A review
journal, December 2010
- Geisseler, Daniel; Horwath, William R.; Joergensen, Rainer Georg
- Soil Biology and Biochemistry, Vol. 42, Issue 12
Forest harvesting reduces the soil metagenomic potential for biomass decomposition
journal, April 2015
- Cardenas, Erick; Kranabetter, J. M.; Hope, Graeme
- The ISME Journal, Vol. 9, Issue 11
Effect of soil moisture status and a nitrification inhibitor, dicyandiamide, on ammonia oxidizer and denitrifier growth and nitrous oxide emissions in a grassland soil
journal, June 2014
- Di, Hong J.; Cameron, Keith C.; Podolyan, Andriy
- Soil Biology and Biochemistry, Vol. 73
The Natural History of Nitrogen Fixation
journal, March 2004
- Raymond, Jason; Siefert, Janet L.; Staples, Christopher R.
- Molecular Biology and Evolution, Vol. 21, Issue 3
Microbial community responses to soil tillage and crop rotation in a corn/soybean agroecosystem
journal, October 2016
- Smith, Chris R.; Blair, Peter L.; Boyd, Charlie
- Ecology and Evolution, Vol. 6, Issue 22
Comparison between the nitric oxide reductase family and its aerobic relatives, the cytochrome oxidases
journal, August 2002
- de Vries, S.; Schröder, I.
- Biochemical Society Transactions, Vol. 30, Issue 4
IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013
- Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
- Nucleic Acids Research, Vol. 42, Issue D1
Biogeography and biophysicochemical traits link N2O emissions, N2O emission potential and microbial communities across New Zealand pasture soils
journal, March 2015
- Morales, Sergio E.; Jha, Neha; Saggar, Surinder
- Soil Biology and Biochemistry, Vol. 82
Ecological Perspectives on Microbes Involved in N-Cycling
journal, January 2014
- Isobe, Kazuo; Ohte, Nobuhito
- Microbes and Environments, Vol. 29, Issue 1
Metagenomic reconstruction of nitrogen cycling pathways in a CO2-enriched grassland ecosystem
journal, March 2017
- Tu, Qichao; He, Zhili; Wu, Liyou
- Soil Biology and Biochemistry, Vol. 106
KEGG as a reference resource for gene and protein annotation
journal, October 2015
- Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki
- Nucleic Acids Research, Vol. 44, Issue D1
A communal catalogue reveals Earth’s multiscale microbial diversity
journal, November 2017
- Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel
- Nature, Vol. 551, Issue 7681
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016
- Letunic, Ivica; Bork, Peer
- Nucleic Acids Research, Vol. 44, Issue W1
Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data: Fig. 1.
journal, May 2015
- Aßhauer, Kathrin P.; Wemheuer, Bernd; Daniel, Rolf
- Bioinformatics, Vol. 31, Issue 17
Nitrogen Cycling in the Ocean: New Perspectives on Processes and Paradigms
journal, March 2002
- Zehr, J. P.; Ward, B. B.
- Applied and Environmental Microbiology, Vol. 68, Issue 3
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions
journal, May 2008
- Galloway, J. N.; Townsend, A. R.; Erisman, J. W.
- Science, Vol. 320, Issue 5878
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils
journal, November 2012
- Sanford, R. A.; Wagner, D. D.; Wu, Q.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 48
Simulated Atmospheric Nitrogen Deposition Alters Actinobacterial Community Composition in Forest Soils
journal, January 2010
- Eisenlord, Sarah D.; Zak, Donald R.
- Soil Science Society of America Journal, Vol. 74, Issue 4
Global biogeography of microbial nitrogen-cycling traits in soil
journal, July 2016
- Nelson, Michaeline B.; Martiny, Adam C.; Martiny, Jennifer B. H.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 29
Complete nitrification by a single microorganism
journal, November 2015
- van Kessel, Maartje A. H. J.; Speth, Daan R.; Albertsen, Mads
- Nature, Vol. 528, Issue 7583
Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli
journal, January 2008
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- Genome Biology, Vol. 9, Issue 1
Genomic Potential for Polysaccharide Deconstruction in Bacteria
journal, December 2014
- Berlemont, Renaud; Martiny, Adam C.
- Applied and Environmental Microbiology, Vol. 81, Issue 4
Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes
journal, January 2012
- Dos Santos, Patricia C.; Fang, Zhong; Mason, Steven W.
- BMC Genomics, Vol. 13, Issue 1
The chemistry of soil organic nitrogen: a review
journal, November 1997
- Schulten, H. -R.; Schnitzer, M.
- Biology and Fertility of Soils, Vol. 26, Issue 1
The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis
journal, December 2004
- Cole, J. R.
- Nucleic Acids Research, Vol. 33, Issue Database issue
Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
journal, November 2017
- Chase, Alexander B.; Karaoz, Ulas; Brodie, Eoin L.
- mBio, Vol. 8, Issue 6
Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed
journal, December 2014
- Rocca, Jennifer D.; Hall, Edward K.; Lennon, Jay T.
- The ISME Journal, Vol. 9, Issue 8
Isolation of an autotrophic ammonia-oxidizing marine archaeon
journal, September 2005
- Könneke, Martin; Bernhard, Anne E.; de la Torre, José R.
- Nature, Vol. 437, Issue 7058
Horizontal gene transfer in evolution: facts and challenges
journal, November 2009
- Boto, Luis
- Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1683
Nitrogen Mineralization: Challenges of a Changing Paradigm
journal, March 2004
- Schimel, Joshua P.; Bennett, Jennifer
- Ecology, Vol. 85, Issue 3
Nitrogenase gene diversity and microbial community structure: a cross-system comparison
journal, July 2003
- Zehr, Jonathan P.; Jenkins, Bethany D.; Short, Steven M.
- Environmental Microbiology, Vol. 5, Issue 7
Nitric oxide reductases in bacteria
journal, August 2000
- Hendriks, Janneke; Oubrie, Arthur; Castresana, Jose
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1459, Issue 2-3
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016
- Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
- Nature Communications, Vol. 7, Issue 1
Bacterial gene abundances as indicators of greenhouse gas emission in soils
journal, February 2010
- Morales, Sergio E.; Cosart, Theodore; Holben, William E.
- The ISME Journal, Vol. 4, Issue 6
Inactivation of gltB Abolishes Expression of the Assimilatory Nitrate Reductase Gene (nasB) in Pseudomonas putida KT2442
journal, June 2000
- Eberl, L.; Ammendola, A.; Rothballer, M. H.
- Journal of Bacteriology, Vol. 182, Issue 12
Metabolic dependencies drive species co-occurrence in diverse microbial communities
journal, May 2015
- Zelezniak, Aleksej; Andrejev, Sergej; Ponomarova, Olga
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill
journal, January 2014
- Mason, Olivia U.; Scott, Nicole M.; Gonzalez, Antonio
- The ISME Journal, Vol. 8, Issue 7
A genomic perspective on stoichiometric regulation of soil carbon cycling
journal, July 2017
- Hartman, Wyatt H.; Ye, Rongzhong; Horwath, William R.
- The ISME Journal, Vol. 11, Issue 12
A new view of the tree of life
journal, April 2016
- Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik
- Nature Microbiology, Vol. 1, Issue 5
Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans.
journal, January 1983
- Carlson, C. A.; Ingraham, J. L.
- Applied and Environmental Microbiology, Vol. 45, Issue 4
Works referencing / citing this record:
Phylogenetic conservation of bacterial responses to soil nitrogen addition across continents
journal, June 2019
- Isobe, Kazuo; Allison, Steven D.; Khalili, Banafshe
- Nature Communications, Vol. 10, Issue 1