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Biogeography of ammonia oxidizers in New England and Gulf of Mexico salt marshes and the potential importance of comammox

  • 1.

    Prosser, J. I. & Nicol, G. W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931–2941 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Bernhard, A. E. & Bollmann, A. Estuarine nitrifiers: new players, patterns and processes. Estuar. Coast. Shelf Sci. 88, 1–11 (2010).

    CAS 
    Article 

    Google Scholar 

  • 3.

    Martiny, J. B. H., Eisen, J., Penn, K., Allison, S. D. & Horner-Devine, M. C. Drivers of bacterial beta-diversity depend on spatial scale. Proc. Natl Acad. Sci. USA 108, 7850–7854 (2011).

  • 4.

    Nelson, M. B., Martiny, A. C. & Martiny, J. B. H. Global biogeography of microbial nitrogen-cycling traits in soil. Proc. Natl Acad. Sci. USA 113, 8033–8040 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 5.

    Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 6.

    Marton, J. M., Roberts, B. J., Bernhard, A. E. & Giblin, A. E. Spatial and temporal variability of nitrification potential and ammonia-oxidizer abundances in Louisiana salt marshes. Estuaries Coast. 38, 1824–1837 (2015).

    CAS 
    Article 

    Google Scholar 

  • 7.

    Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461, 976–981 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 8.

    Dimitri Kits, K. et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549, 269–272 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 9.

    Hink, L., Nicol, G. W. & Prosser, J. I. Archaea produce lower yields of N<inf>2</inf>O than bacteria during aerobic ammonia oxidation in soil. Environ. Microbiol. 19, 4829–4837 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 10.

    Bernhard, A. E., Donn, T., Giblin, A. E. & Stahl, D. A. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ. Microbiol. 7, 1289–1297 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    Moin, N. S., Nelson, K. A., Bush, A. & Bernhard, A. E. Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl. Environ. Microbiol. 75, 7461–7468 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 12.

    Bernhard, A. E. et al. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl. Environ. Microbiol. 76, 1285–1289 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 13.

    Francis, C. A., O’Mullan, G. D. & Ward, B. B. Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1, 129–140 (2003).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Ward, B. B. et al. Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray. Environ. Microbiol. 9, 2522–2538 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 15.

    Mills, H. J. et al. Characterization of nitrifying, denitrifying, and overall bacterial communities in permeable marine sediments of the northeastern Gulf of Mexico. Appl. Environ. Microbiol. 74, 4440–4453 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 16.

    Newell, S. E. et al. A shift in the archaeal nitrifier community in response to natural and anthropogenic disturbances in the northern Gulf of Mexico. Environ. Microbiol. Rep. 6, 106–112 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 17.

    Bernhard, A. E., Sheffer, R., Giblin, A. E., Marton, J. M. & Roberts, B. J. Population dynamics and community composition of ammonia oxidizers in salt marshes after the Deepwater Horizon oil spill. Front. Microbiol. 7, 854 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 18.

    Bernhard, A. E., Chelsky, A., Giblin, A. E. & Roberts, B. J. Influence of local and regional drivers on spatial and temporal variation of ammonia-oxidizing communities in Gulf of Mexico salt marshes. Environ. Microbiol. Rep. 11, 825–834 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 19.

    Nelson, K. A., Moin, N. S. & Bernhard, A. E. Archaeal diversity and the prevalence of Crenarchaeota in salt marsh sediments. Appl. Environ. Microbiol. 75, 4211–4215 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 20.

    Peng, X. et al. Differential responses of ammonia-oxidizing archaea and bacteria to long-term fertilization in a New England salt marsh. Front. Microbiol. 3, 445 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 21.

    Bernhard, A. E., Marshall, D. & Yiannos, L. Increased variability of microbial communities in restored salt marshes nearly 30 years after tidal flow restoration. Estuaries Coast. 35, 1049–1059 (2012).

    CAS 
    Article 

    Google Scholar 

  • 22.

    Marton, J. M. & Roberts, B. J. Spatial variability of phosphorus sorption dynamics in Louisiana salt marshes. J. Geophys. Res. Biogeosci. 119, 451–465 (2014).

    CAS 
    Article 

    Google Scholar 

  • 23.

    Hill, T. D. & Roberts, B. J. Effects of seasonality and environmental gradients on Spartina alterniflora allometry and primary production. Ecol. Evol. 7, 9676–9688 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 24.

    Bernhard, A. E., Tucker, J., Giblin, A. E. & Stahl, D. A. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ. Microbiol. 9, 1439–1447 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 25.

    Schutte, C. A., Marton, J. M., Bernhard, A. E., Giblin, A. E. & Roberts, B. J. No evidence for long-term impacts of oil spill contamination on salt marsh soil nitrogen cycling processes. Estuaries Coast. 43, 865–879 (2020).

    Article 

    Google Scholar 

  • 26.

    Bernhard, A. E., Dwyer, C., Idrizi, A., Bender, G. & Zwick, R. Long-term impacts of disturbance on nitrogen-cycling bacteria in a New England salt marsh. Front. Microbiol. 6 https://doi.org/10.3389/fmicb.2015.00046 (2015).

  • 27.

    Pjevac, P. et al. AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front. Microbiol. 8 https://doi.org/10.3389/fmicb.2017.01508 (2017).

  • 28.

    Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E. & Oakley, B. B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl Acad. Sci. USA 102, 14683–14688 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Park, S.-J., Park, B.-J. & Rhee, S.-K. Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles 12, 605–615 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 30.

    Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 31.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 32.

    Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 33.

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  • 34.

    Turner, R. E., Rabalais, N. N. & Justic, D. Predicting summer hypoxia in the northern Gulf of Mexico: riverine N, P, and Si loading. Mar. Pollut. Bull. 52, 139–148 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 35.

    Tian, H. et al. Long-term trajectory of nitrogen loading and delivery from Mississippi river basin to the Gulf of Mexico. Glob. Biogeochem. Cycles 34, 6475 (2020).

    Article 
    CAS 

    Google Scholar 

  • 36.

    Dang, H. et al. Diversity, abundance, and spatial distribution of sedimet ammonia-oxidizing Betaproteobacteria in response to environmental gradients and coastal eutrophication in Jiaozhou Bay, China. Appl. Environ. Microbiol. 76, 4691–4702 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 37.

    Sims, A., Zhang, Y., Gajaraj, S., Brown, P. B. & Hu, Z. Toward the development of microbial indicators for wetland assessment. Water Res. 47, 1711–1725 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 38.

    Zhang, Q. -F. et al. Impacts of Spartina alterniflora invasion on abundance and composition of ammonia oxidizers in estuarine sediment. J. Soils Sediment. 11, 1020–1031 (2011).

    Article 

    Google Scholar 

  • 39.

    Jin, T. et al. Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River Estuary, China. Appl. Microbiol. Biotechnol. 90, 1137–1145 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 40.

    Meinhardt, K. A. et al. Evaluation of revised polymerase chain reaction primers for more inclusive quantification of ammonia-oxidizing archaea and bacteria. Environ. Microbiol. Rep. 7, 354–363 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 41.

    Marshall, A. et al. Primer selection influences abundance estimates of ammonia oxidizing archaea in coastal marine sediments. Mar. Environ. Res. 140, 90–95 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Koops, H. P. & Pommerening-Roser, A. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37, 1–9 (2001).

    CAS 
    Article 

    Google Scholar 

  • 43.

    Hillebrand, H. On the generality of the latitudinal diversity gradient. Am. Nat. 163, 192–211 (2004).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 44.

    Pommier, T. et al. Global patterns of diversity and community structure in marine bacterioplankton. Mol. Ecol. 16, 867–880 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. 103, 626–631 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 46.

    Hendershot, J. N., Read, Q. D., Henning, J. A., Sanders, N. J. & Classen, A. T. Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98, 1757–1763 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 47.

    Hitchcock, J. N., Mitrovic, S. M., Kobayashi, T. & Westhorpe, D. P. Responses of estuarine bacterioplankton, phytoplankton and zooplankton to dissolved organic carbon (DOC) and inorganic nutrient additions. Estuaries Coast. 33, 78–91 (2010).

    CAS 
    Article 

    Google Scholar 

  • 48.

    Guo, X. -P. et al. Bacterial community structure in response to environmental impacts in the intertidal sediments along the Yangtze Estuary, China. Mar. Pollut. Bull. 126, 141–149 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 49.

    Howarth, R. W. Nutrient limitation of net primary production in marine ecosystems. Annu. Rev. Ecol. 19, 89–110 (1988).

    Article 

    Google Scholar 

  • 50.

    Murrell, M. C. et al. Evidence that phosphorus limits phytoplankton growth in a Gulf of Mexico estuary: Pensacola Bay, Florida, USA. Bull. Mar. Sci. 70, 155–167 (2002).

    Google Scholar 

  • 51.

    Johnson, M. W., Heck, K. L. Jr & Fourqurean, J. W. Nutrient content of seagrasses and epiphytes in the northern Gulf of Mexico: evidence of phosphorus and nitrogen limitation. Aquat. Bot. 85, 103–111 (2006).

    CAS 
    Article 

    Google Scholar 

  • 52.

    Rysgaard, S., Thastum, P., Dalsgaard, T., Christensen, P. B. & Sloth, N. P. Effects of salinity on NH4+ adsorption capacity, nitrification, and denitrification in Danish estuarine sediments. Estuaries 22, 21–30 (1999).

    CAS 
    Article 

    Google Scholar 

  • 53.

    Peng, X. et al. Long-term fertilization alters the relative importance of nitrate reduction pathways in salt marsh sediments. J. Geophys. Res. Biogeosci. 121, 2082–2095 (2016).

    CAS 
    Article 

    Google Scholar 

  • 54.

    Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article 

    Google Scholar 

  • 55.

    Taylor, A. E., Giguere, A. T., Zoebelein, C. M., Myrold, D. D. & Bottomley, P. J. Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME J. 11, 896–908 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 56.

    Ouyang, Y., Norton, J. M. & Stark, J. M. Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil. Soil Biol. Biochem. 113, 161–172 (2017).

    CAS 
    Article 

    Google Scholar 

  • 57.

    Mukhtar, H., Lin, Y. -P., Lin, C. -M. & Lin, Y. -R. Relative abundance of ammonia oxidizing archaea and bacteria influences soil nitrification responses to temperature. Microorganisms 7, 526 (2019).

    Google Scholar 

  • 58.

    Fierer, N., Carney, K. M., Horner-Devine, M. C. & Megonigal, J. P. The biogeography of ammonia-oxidizing bacterial communities in soil. Microb. Ecol. 58, 435–445 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 59.

    Park, H.-D., Lee, S.-Y. & Hwang, S. Redundancy analysis demonstration of the relevance of temperature to ammonia-oxidizing bacterial community compositions in a full-scale nitrifying bioreactor treating saline wastewater. J. Microbiol. Biotechnol. 19, 346–350 (2009).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 60.

    Avrahami, S., Liesack, W. & Conrad, R. Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ. Microbiol. 5, 691–705 (2003).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 61.

    Avrahami, S. & Conrad, R. Patterns of community change among ammonia oxidizers in meadow soils upon long-term incubation at different temperatures. Appl. Environ. Microbiol. 69, 6152–6164 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 62.

    Seitzinger, S. P., Gardner, W. S. & Spratt, A. K. The effect of salinity on ammonium sorption in aquatic sediments—implications for benthic nutrient recycling. Estuaries 14, 167–174 (1991).

    CAS 
    Article 

    Google Scholar 

  • 63.

    Dollhopf, S. L. et al. Quantification of ammonia-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Appl. Environ. Microbiol. 71, 240–246 (2005).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 64.

    Beman, J. M., Bertics, V. J., Braunschweiler, T. & Wilson, J. M. Quantification of ammonia oxidation rates and the distribution of ammonia-oxidizing archaea and bacteria in marine sediment depth profiles from Catalina Island, California. Front. Microbiol. 3, 263 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 65.

    Nicol, G. W., Leininger, S., Schleper, C. & Prosser, J. I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966–2978 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 66.

    Lehtovirta, L. E., Prosser, J. I. & Nicol, G. W. Soil pH regulates the abundance and diversity of group 1.1c Crenarchaeota. FEMS Microbiol. Ecol. 70, 367–376 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 67.

    Bello, M. O., Thion, C., Gubry-Rangin, C. & Prosser, J. I. Differential sensitivity of ammonia oxidising archaea and bacteria to matric and osmotic potential. Soil Biol. Biochem. 129, 184–190 (2019).

    CAS 
    Article 

    Google Scholar 

  • 68.

    Fuchslueger, L. et al. Effects of drought on nitrogen turnover and abundances of ammonia-oxidizers in mountain grassland. Biogeosciences. 11, 6003–6015 (2014).

    Article 

    Google Scholar 

  • 69.

    Thion, C. & Prosser, J. I. Differential response of nonadapted ammonia-oxidising archaea and bacteria to drying-rewetting stress. FEMS Microbiol. Ecol. 90, 380–389 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 70.

    Fowler, S. J., Palomo, A., Dechesne, A., Mines, P. D. & Smets, B. F. Comammox Nitrospira are abundant ammonia oxidizers in diverse groundwater-fed rapid sand filter communities. Environ. Microbiol. 20, 1002–1015 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    How, S. W., Chua, A. S. M., Ngoh, G. C., Nittami, T. & Curtis, T. P. Enhanced nitrogen removal in an anoxic-oxic-anoxic process treating low COD/N tropical wastewater: low-dissolved oxygen nitrification and utilization of slowly-biodegradable COD for denitrification. Sci. Total Environ. 693, 133526 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Gonzalez-Martinez, A., Rodriguez-Sanchez, A., van Loosdrecht, M. C. M., Gonzalez-Lopez, J. & Vahala, R. Detection of comammox bacteria in full-scale wastewater treatment bioreactors using tag-454-pyrosequencing. Environ. Sci. Pollut. Res. 23, 25501–25511 (2016).

    CAS 
    Article 

    Google Scholar 

  • 73.

    Wang, D. -Q., Zhou, C. -H., Nie, M., Gu, J. -D. & Quan, Z. -X. Abundance and niche specificity of different types of complete ammonia oxidizers (comammox) in salt marshes covered by different plants. Sci. Total Environ. 768, 144933 (2021).

    Google Scholar 

  • 74.

    Xia, F. et al. Ubiquity and diversity of complete ammonia oxidizers (comammox). Appl. Environ. Microbiol. 84, e01390 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 75.

    Yu, C. et al. Evidence for complete nitrification in enrichment culture of tidal sediments and diversity analysis of clade a comammox Nitrospira in natural environments. Appl. Microbiol. Biotechnol. 102, 9363–9377 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 76.

    Zhao, Z. et al. Abundance and community composition of comammox bacteria in different ecosystems by a universal primer set. Sci. Total Environ. 691, 146–155 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 


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