Evaluation of revised polymerase chain reaction primers for more inclusive quantification of ammonia‐oxidizing archaea and bacteria

Meinhardt, Kelley A.; Bertagnolli, Anthony; Pannu, Manmeet W.; Strand, Stuart E.; Brown, Sally L.; Stahl, David A.

doi:10.1111/1758-2229.12259

Evaluation of revised polymerase chain reaction primers for more inclusive quantification of ammonia‐oxidizing archaea and bacteria

Journal Article · Thu Feb 12 00:00:00 EST 2015 · Environmental Microbiology Reports

DOI:https://doi.org/10.1111/1758-2229.12259· OSTI ID:1400677

Meinhardt, Kelley A. ^[1]; Bertagnolli, Anthony ^[1]; Pannu, Manmeet W. ^[1]; Strand, Stuart E. ^[1]; Brown, Sally L. ^[2]; Stahl, David A. ^[1]

Civil and Environmental Engineering University of Washington Seattle WA 98105 USA
School of Environmental and Forest Sciences University of Washington Seattle WA 98105 USA

Summary

Ammonia‐oxidizing archaea ( AOA ) and bacteria ( AOB ) fill key roles in the nitrogen cycle. Thus, well‐vetted methods for characterizing their distribution are essential for framing studies of their significance in natural and managed systems. Quantification of the gene coding for one subunit of the ammonia monooxygenase ( amoA ) by polymerase chain reaction is frequently employed to enumerate the two groups. However, variable amplification of sequence variants comprising this conserved genetic marker for ammonia oxidizers potentially compromises within‐ and between‐system comparisons. We compared the performance of newly designed non‐degenerate quantitative polymerase chain reaction primer sets to existing primer sets commonly used to quantify the amoA of AOA and AOB using a collection of plasmids and soil DNA samples. The new AOA primer set provided improved quantification of model mixtures of different amoA sequence variants and increased detection of amoA in DNA recovered from soils. Although both primer sets for the AOB provided similar results for many comparisons, the new primers demonstrated increased detection in environmental application. Thus, the new primer sets should provide a useful complement to primers now commonly used to characterize the environmental distribution of AOA and AOB .

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0006869

OSTI ID:: 1400677

Journal Information:: Environmental Microbiology Reports, Journal Name: Environmental Microbiology Reports Journal Issue: 2 Vol. 7; ISSN 1758-2229

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United States

Language:: English

References (35)

The Nature and Longevity of Agricultural Impacts on Soil Carbon and Nutrients: A Review McLauchlan, Kendra Ecosystems, Vol. 9, Issue 8 https://doi.org/10.1007/s10021-005-0135-1	journal	December 2006
Review of greenhouse gas emissions from crop production systems and fertilizer management effects Snyder, C. S.; Bruulsema, T. W.; Jensen, T. L. Agriculture, Ecosystems & Environment, Vol. 133, Issue 3-4 https://doi.org/10.1016/j.agee.2009.04.021	journal	October 2009
Effect of nitrification inhibitors on the growth and activity of Nitrosotalea devanaterra in culture and soil Lehtovirta-Morley, Laura E.; Verhamme, Daniël T.; Nicol, Graeme W. Soil Biology and Biochemistry, Vol. 62 https://doi.org/10.1016/j.soilbio.2013.01.020	journal	July 2013
Calculator Tool for Determining Greenhouse Gas Emissions for Biosolids Processing and End Use Brown, Sally; Beecher, Ned; Carpenter, Andrew Environmental Science & Technology, Vol. 44, Issue 24 https://doi.org/10.1021/es101210k	journal	December 2010
Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea Alves, Ricardo J. Eloy; Wanek, Wolfgang; Zappe, Anna The ISME Journal, Vol. 7, Issue 8 https://doi.org/10.1038/ismej.2013.35	journal	March 2013
Isolation of an autotrophic ammonia-oxidizing marine archaeon Könneke, Martin; Bernhard, Anne E.; de la Torre, José R. Nature, Vol. 437, Issue 7058 https://doi.org/10.1038/nature03911	journal	September 2005
Archaea predominate among ammonia-oxidizing prokaryotes in soils Leininger, S.; Urich, T.; Schloter, M. Nature, Vol. 442, Issue 7104 https://doi.org/10.1038/nature04983	journal	August 2006
Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria Martens-Habbena, Willm; Berube, Paul M.; Urakawa, Hidetoshi Nature, Vol. 461, Issue 7266 https://doi.org/10.1038/nature08465	journal	September 2009
Solutions for a cultivated planet Foley, Jonathan A.; Ramankutty, Navin; Brauman, Kate A. Nature, Vol. 478, Issue 7369 https://doi.org/10.1038/nature10452	journal	October 2011
Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils Di, H. J.; Cameron, K. C.; Shen, J. P. Nature Geoscience, Vol. 2, Issue 9 https://doi.org/10.1038/ngeo613	journal	August 2009
Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean Francis, C. A.; Roberts, K. J.; Beman, J. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 41, p. 14683-14688 https://doi.org/10.1073/pnas.0506625102	journal	September 2005
A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring Hatzenpichler, R.; Lebedeva, E. V.; Spieck, E. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0708857105	journal	February 2008
Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil Tourna, M.; Stieglmeier, M.; Spang, A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 20 https://doi.org/10.1073/pnas.1013488108	journal	April 2011
Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil Lehtovirta-Morley, L. E.; Stoecker, K.; Vilcinskas, A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 38 https://doi.org/10.1073/pnas.1107196108	journal	September 2011
Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation Qin, W.; Amin, S. A.; Martens-Habbena, W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 34 https://doi.org/10.1073/pnas.1324115111	journal	August 2014
The degenerate primer design problem Linhart, C.; Shamir, R. Bioinformatics, Vol. 18, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/18.suppl_1.S172	journal	July 2002
Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling: Role of mesophilic crenarchaeota in nitrogen cycling Treusch, Alexander H.; Leininger, Sven; Kletzin, Arnulf Environmental Microbiology, Vol. 7, Issue 12 https://doi.org/10.1111/j.1462-2920.2005.00906.x	journal	September 2005
Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples Smith, Cindy J.; Nedwell, David B.; Dong, Liang F. Environmental Microbiology, Vol. 8, Issue 5 https://doi.org/10.1111/j.1462-2920.2005.00963.x	journal	May 2006
Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre Mincer, Tracy J.; Church, Matthew J.; Taylor, Lance Trent Environmental Microbiology, Vol. 9, Issue 5 https://doi.org/10.1111/j.1462-2920.2007.01239.x	journal	May 2007
Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices He, Ji-zheng; Shen, Ju-pei; Zhang, Li-mei Environmental Microbiology, Vol. 9, Issue 9 https://doi.org/10.1111/j.1462-2920.2007.01358.x	journal	September 2007
Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol de la Torre, José R.; Walker, Christopher B.; Ingalls, Anitra E. Environmental Microbiology, Vol. 10, Issue 3 https://doi.org/10.1111/j.1462-2920.2007.01506.x	journal	March 2008
Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon Boyle-Yarwood, Stephanie A.; Bottomley, Peter J.; Myrold, David D. Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01600.x	journal	November 2008
The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria Nicol, Graeme W.; Leininger, Sven; Schleper, Christa Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01701.x	journal	November 2008
Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil Jia, Zhongjun; Conrad, Ralf Environmental Microbiology, Vol. 11, Issue 7 https://doi.org/10.1111/j.1462-2920.2009.01891.x	journal	July 2009
amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions: Archaeal amoA phylogeny and diversity in soils Pester, Michael; Rattei, Thomas; Flechl, Stefan Environmental Microbiology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1462-2920.2011.02666.x	journal	December 2011
Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska: Functional genes predict potential N cycling rates Petersen, Dorthe Groth; Blazewicz, Steven J.; Firestone, Mary Environmental Microbiology, Vol. 14, Issue 4 https://doi.org/10.1111/j.1462-2920.2011.02679.x	journal	January 2012
High abundance of Crenarchaeota in a temperate acidic forest soil: Highly abundant Crenarchaeota in a forest soil Kemnitz, Dana; Kolb, Steffen; Conrad, Ralf FEMS Microbiology Ecology, Vol. 60, Issue 3 https://doi.org/10.1111/j.1574-6941.2007.00310.x	journal	June 2007
Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene: Archaeal ammonia oxidation in soil Offre, Pierre; Prosser, James I.; Nicol, Graeme W. FEMS Microbiology Ecology, Vol. 70, Issue 1 https://doi.org/10.1111/j.1574-6941.2009.00725.x	journal	October 2009
Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest Zhang, Li-Mei; Wang, Mu; Prosser, James I. FEMS Microbiology Ecology, Vol. 70, Issue 2 https://doi.org/10.1111/j.1574-6941.2009.00775.x	journal	November 2009
Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile: Selection of ammonia oxidizers in wetland soil Höfferle, Špela; Nicol, Graeme W.; Pal, Levin FEMS Microbiology Ecology, Vol. 74, Issue 2 https://doi.org/10.1111/j.1574-6941.2010.00961.x	journal	August 2010
Archaea rather than bacteria control nitrification in two agricultural acidic soils: Archaeal nitrification in acidic soils Gubry-Rangin, Cécile; Nicol, Graeme W.; Prosser, James I. FEMS Microbiology Ecology, Vol. 74, Issue 3 https://doi.org/10.1111/j.1574-6941.2010.00971.x	journal	October 2010
Distinct Responses in Ammonia-Oxidizing Archaea and Bacteria after Addition of Biosolids to an Agricultural Soil Kelly, John J.; Policht, Katherine; Grancharova, Tanya Applied and Environmental Microbiology, Vol. 77, Issue 18 https://doi.org/10.1128/AEM.02608-10	journal	July 2011
Archaea Dominate the Ammonia-Oxidizing Community in the Rhizosphere of the Freshwater Macrophyte Littorella uniflora Herrmann, M.; Saunders, A. M.; Schramm, A. Applied and Environmental Microbiology, Vol. 74, Issue 10 https://doi.org/10.1128/AEM.02802-07	journal	March 2008
The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Rotthauwe, J. H.; Witzel, K. P.; Liesack, W. Applied and environmental microbiology, Vol. 63, Issue 12 https://doi.org/10.1128/AEM.63.12.4704-4712.1997	journal	January 1997
Bias in Template-to-Product Ratios in Multitemplate PCR Polz, Martin F.; Cavanaugh, Colleen M. Applied and Environmental Microbiology, Vol. 64, Issue 10 https://doi.org/10.1128/AEM.64.10.3724-3730.1998	journal	October 1998

Similar Records

Influence of edaphic and management factors on the diversity and abundance of ammonia‐oxidizing thaumarchaeota and bacteria in soils of bioenergy crop cultivars

Journal Article · Wed Feb 25 19:00:00 EST 2015 · Environmental Microbiology Reports · OSTI ID:1400890

TESTING THE SPECIFICITY OF PRIMERS TO ENVIRONMENTAL AMMONIA MONOOXYGENASE (AMOA) GENES IN GROUNDWATER TREATED WITH UREA TO PROMOTE CALCITE PRECIPITATION

Journal Article · Thu Nov 30 23:00:00 EST 2006 · DOE Journal of Undergraduate Research · OSTI ID:926763

Testing the Specificity of Primers to Environmental Ammonia Monooxygenase (amoA) Genes in Groundwater Treated with Urea to Promote Calcite Precipitation

Journal Article · Sat Dec 31 23:00:00 EST 2005 · Journal of Undergraduate Research · OSTI ID:1051817

Evaluation of revised polymerase chain reaction primers for more inclusive quantification of ammonia‐oxidizing archaea and bacteria

Citation Formats

References (35)

Similar Records

Related Subjects