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:
-
- 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}
}
Web of Science
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