Deep amoA amplicon sequencing reveals community partitioning within ammonia-oxidizing bacteria in the environmentally dynamic estuary of the River Elbe

Kowalchuk, G. A. & Stephen, J. R. Ammonia-oxidizing bacteria: A model for molecular microbial ecology. Annu. Rev. Microbiol. 55, 485–529. https://doi.org/10.1146/annurev.micro.55.1.485 (2001).

CAS  Article  PubMed  Google Scholar 

Koops, H.-P. & Pommerening-Röser, A. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37, 1–9. https://doi.org/10.1111/j.1574-6941.2001.tb00847.x (2001).

CAS  Article  Google Scholar 

Monteiro, M., Seneca, J. & Magalhaes, C. The history of aerobic ammonia oxidizers: From the first discoveries to today. J. Microbiol. 52, 537–547. https://doi.org/10.1007/s12275-014-4114-0 (2014).

CAS  Article  PubMed  Google Scholar 

Lehtovirta-Morley, L. E. Ammonia oxidation: Ecology, physiology, biochemistry and why they must all come together. FEMS Microbiol. Lett. https://doi.org/10.1093/femsle/fny058 (2018).

Article  PubMed  Google Scholar 

Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543. https://doi.org/10.1038/nature03911 (2005).

ADS  CAS  Article  PubMed  Google Scholar 

Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504. https://doi.org/10.1038/nature16461 (2015).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

van Kessel, M. A. H. J. et al. Complete nitrification by a single microorganism. Nature 528, 555. https://doi.org/10.1038/nature16459 (2015).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809. https://doi.org/10.1038/nature04983 (2006).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

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, 976–979. https://doi.org/10.1038/nature08465 (2009).

ADS  CAS  Article  PubMed  Google Scholar 

Prosser, J. I. & Nicol, G. W. Archaeal and bacterial ammonia-oxidisers in soil: The quest for niche specialisation and differentiation. Trends Microbiol. 20, 523–531. https://doi.org/10.1016/j.tim.2012.08.001 (2012).

CAS  Article  PubMed  Google Scholar 

Shen, J. P., Zhang, L. M., Zhu, Y. G., Zhang, J. B. & He, J. Z. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ. Microbiol. 10, 1601–1611. https://doi.org/10.1111/j.1462-2920.2008.01578.x (2008).

CAS  Article  PubMed  Google Scholar 

Tourna, M., Freitag, T. E., Nicol, G. W. & Prosser, J. I. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10, 1357–1364. https://doi.org/10.1111/j.1462-2920.2007.01563.x (2008).

CAS  Article  PubMed  Google Scholar 

Verhamme, D. T., Prosser, J. I. & Nicol, G. W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067–1071. https://doi.org/10.1038/ismej.2010.191 (2011).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Wang, Y. F., Li, X. Y. & Gu, J. D. Differential responses of ammonia/ammonium-oxidizing microorganisms in mangrove sediment to amendment of acetate and leaf litter. Appl. Microbiol. Biotechnol. 98, 3165–3180. https://doi.org/10.1007/s00253-013-5318-7 (2014).

CAS  Article  PubMed  Google Scholar 

Sahan, E. & Muyzer, G. Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol. Ecol. 64, 175–186. https://doi.org/10.1111/j.1574-6941.2008.00462.x (2008).

CAS  Article  PubMed  Google Scholar 

Saha, M., Sarkar, A. & Bandhophadhyay, B. Introduction to establish the comparative analysis of 16S rRNA gene sequences with amoA and nxrA for nitrifying bacteria isolated from East Kolkata wetland: An International Ramsar Site. J. Aquac. Res. Dev. https://doi.org/10.4172/2155-9546.1000270 (2014).

Article  Google Scholar 

Watson, S. W. Characteristics of a marine nitrifying bacterium, Nitrosocystis oceanus sp. n.. Limnol. Oceanogr. 10, 274–289 (1965).

ADS  Article  Google Scholar 

Campbell, M. A. et al. Nitrosococcus watsonii sp. nov., a new species of marine obligate ammonia-oxidizing bacteria that is not omnipresent in the world’s oceans: Calls to validate the names ‘Nitrosococcus halophilus’ and ‘Nitrosomonas mobilis’. FEMS Microbiol. Ecol. 76, 39–48. https://doi.org/10.1111/j.1574-6941.2010.01027.x (2011).

CAS  Article  PubMed  Google Scholar 

Hayatsu, M. et al. An acid-tolerant ammonia-oxidizing gamma-proteobacterium from soil. ISME J. 11, 1130–1141. https://doi.org/10.1038/ismej.2016.191 (2017).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Koops, H.-P., Böttcher, B., Möller, U. C., Pommerening-Röser, A. & Stehr, G. Description of a new species of Nitrosococcus. Arch. Microbiol. 154, 244–248. https://doi.org/10.1007/bf00248962 (1990).

CAS  Article  Google Scholar 

Garrity, G. M., Bell, J. A., Lilburn, T. F. & I. , Nitrosomonadaceae fam nov. In Bergey’s Manual of Systematic Bacteriology, second edition, vol. 2 (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria) (eds Brenner, D. J. et al.) 864 (Springer, New York, 2006).

Google Scholar 

Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996. https://doi.org/10.1038/nbt.4229 (2018).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Schoer, J. H. Determination of the origin of suspended matter and sediments in the Elbe Estuary using natural tracers. Estuaries 13, 161–172. https://doi.org/10.2307/1351585 (1990).

CAS  Article  Google Scholar 

Groengroeft, A. et al. Distribution of metals in sediments of the Elbe estuary in 1994. Water Sci. Technol. 37, 109–116. https://doi.org/10.1016/S0273-1223(98)00189-9 (1998).

CAS  Article  Google Scholar 

Kleisinger, C., Haase, H., Hentschke, U. & Schubert, B. Contamination of sediments in the German North Sea Estuaries Elbe, Weser and Ems and its sensitivity to climate change. In (eds. Heiniger P. & Cullmann J.) 129–149 (Springer International Publishing, Geneva, 2015).

Reese, A., Zimmermann, T., Profrock, D. & Irrgeher, J. Extreme spatial variation of Sr, Nd and Pb isotopic signatures and 48 element mass fractions in surface sediment of the Elbe River Estuary—Suitable tracers for processes in dynamic environments?. Sci. Total Environ. 668, 512–523. https://doi.org/10.1016/j.scitotenv.2019.02.401 (2019).

ADS  CAS  Article  PubMed  Google Scholar 

Rotthauwe, J. H., Witzel, K. P. & Liesack, W. The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704–4712 (1997).

CAS  Article  Google Scholar 

Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17(3), 2011. https://doi.org/10.14806/ej.17.1.200 (2011).

Article  Google Scholar 

Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 4, e2584. https://doi.org/10.7717/peerj.2584 (2016).

Article  PubMed  PubMed Central  Google Scholar 

Šmilauer, P. & Lepš, J. Multivariate Analysis of Ecological Data using CANOCO 5 2nd edn. (Cambridge University Press, Cambridge, 2014).

Google Scholar 

Hammer, Ø, Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).

Google Scholar 

Holmes, A. J., Costello, A., Lidstrom, M. E. & Murrell, J. C. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132, 203–208. https://doi.org/10.1016/0378-1097(95)00311-r (1995).

CAS  Article  PubMed  Google Scholar 

Okano, Y. et al. Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl. Environ. Microbiol. 70, 1008–1016. https://doi.org/10.1128/aem.70.2.1008-1016.2004 (2004).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Stehr, G., Böttcher, B., Dittberner, P., Rath, G. & Koops, H.-P. The ammonia-oxidizing nitrifying population of the River Elbe estuary. FEMS Microbiol. Ecol. 17, 177–186. https://doi.org/10.1016/0168-6496(95)00022-3 (1995).

CAS  Article  Google Scholar 

Koops, H. P., Böttcher, B., Möller, U. C., Pommerening-Röser, A. & Stehr, G. Classification of eight new species of ammonia-oxidizing bacteria: Nitrosomonas communis sp. nov., Nitrosomonas ureae sp. nov., Nitrosomonas aestuarii sp. nov., Nitrosomonas marina sp. nov., Nitrosomonas nitrosa sp. nov., Nitrosomonas eutropha sp. nov., Nitrosomonas oligotropha sp. nov. and Nitrosomonas halophila sp. nov.. Microbiology 137, 1689–1699. https://doi.org/10.1099/00221287-137-7-1689 (1991).

CAS  Article  Google Scholar 

Suwa, Y., Sumino, T. & Noto, K. Phylogenetic relationships of activated sludge isolates of ammonia oxidizers with different sensitivities to ammonium sulfate. J. Gen. Appl. Microbiol. 43, 373–379 (1997).

CAS  Article  Google Scholar 

Koops, H. P., Purkhold, U., Pommerening-Roser, A., Timmermann, G. & Wagner, M. The lithoautotrophic ammonia-oxidizing bacteria. In The Prokaryotes: An Evoluting Electronic Resource for the Microbiological Community (ed. Dworkin, M.) (Springer, New York, 2003).

Google Scholar 

Ballinger, S. J., Head, I. M., Curtis, T. P. & Godley, A. R. Molecular microbial ecology of nitrification in an activated sludge process treating refinery wastewater. Water Sci. Technol. 37, 105–108. https://doi.org/10.1016/S0273-1223(98)00091-2 (1998).

CAS  Article  Google Scholar 

Gieseke, A., Purkhold, U., Wagner, M., Amann, R. & Schramm, A. Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl. Environ. Microbiol. 67, 1351–1362. https://doi.org/10.1128/aem.67.3.1351-1362.2001 (2001).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Dionisi, H. M. et al. Quantification of Nitrosomonas oligotropha-like ammonia-oxidizing bacteria and Nitrospira spp. from full-scale wastewater treatment plants by competitive PCR. Appl. Environ. Microbiol. 68, 245–253. https://doi.org/10.1128/AEM.68.1.245-253.2002 (2002).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Harms, G. et al. Real-time PCR quantification of nitrifying bacteria in a municipal wastewater treatment plant. Environ. Sci. Technol. 37, 343–351. https://doi.org/10.1021/es0257164 (2003).

ADS  CAS  Article  PubMed  Google Scholar 

Qin, Y. Y., Li, D. T. & Yang, H. Investigation of total bacterial and ammonia-oxidizing bacterial community composition in a full-scale aerated submerged biofilm reactor for drinking water pretreatment in China. FEMS Microbiol. Lett. 268, 126–134. https://doi.org/10.1111/j.1574-6968.2006.00571.x (2007).

CAS  Article  PubMed  Google Scholar 

Regan, J. M., Harrington, G. W. & Noguera, D. R. Ammonia- and nitrite-oxidizing bacterial communities in a pilot-scale chloraminated drinking water distribution system. Appl. Environ. Microbiol. 68, 73–81 (2002).

CAS  Article  Google Scholar 

Stehr, G. et al. Exopolymers: An ecological characteristic of a floc-attached, ammonia-oxidizing bacterium. Microb. Ecol. 30, 115–126 (1995).

CAS  Article  Google Scholar 

Bollmann, A. & Laanbroek, H. J. Influence of oxygen partial pressure and salinity on the community composition of ammonia-oxidizing bacteria in the Schelde estuary. Aquat. Microb. Ecol. 28, 239–247 (2002).

Article  Google Scholar 

Cébron, A., Coci, M., Garnier, J. & Laanbroek, H. J. Denaturing gradient gel electrophoretic analysis of ammonia-oxidizing bacterial community structure in the lower Seine River: Impact of Paris wastewater effluents. Appl. Environ. Microbiol. 70, 6726–6737. https://doi.org/10.1128/aem.70.11.6726-6737.2004 (2004).

Article  PubMed  PubMed Central  Google Scholar 

Cao, H., Hong, Y., Li, M. & Gu, J. D. Community shift of ammonia-oxidizing bacteria along an anthropogenic pollution gradient from the Pearl River Delta to the South China Sea. Appl. Microbiol. Biotechnol. 94, 247–259. https://doi.org/10.1007/s00253-011-3636-1 (2012).

CAS  Article  PubMed  Google Scholar 

Limpiyakorn, T., Shinohara, Y., Kurisu, F. & Yagi, O. Communities of ammonia-oxidizing bacteria in activated sludge of various sewage treatment plants in Tokyo. FEMS Microbiol. Ecol. 54, 205–217. https://doi.org/10.1016/j.femsec.2005.03.017 (2005).

CAS  Article  PubMed  Google Scholar 

Winogradsky, S. & Winogradsky, H. Etudes sur la microbiologie du sol. VII Nouvelles recherches sur les organismes de la nitrification. Ann. Inst Pasteur 50, 350–432 (1933).

Google Scholar 

Watson, S. W. Reisolation of Nitrosospira briensis S. Winogradsky and H. Winogradsky 1933. Archiv fur Mikrobiologie 75, 179–188. https://doi.org/10.1007/bf00408979 (1971).

CAS  Article  PubMed  Google Scholar 

Urakawa, H. et al. Nitrosospira lacus sp. nov., a psychrotolerant, ammonia-oxidizing bacterium from sandy lake sediment. Int. J. Syst. Evol. Microbiol. 65, 242–250. https://doi.org/10.1099/ijs.0.070789-0 (2015).

CAS  Article  PubMed  Google Scholar 

Harms, H., Koops, H. P. & Wehrmann, H. An ammonia-oxidizing bacterium, Nitrosovibrio tenuis nov. gen. nov. sp. Arch. Microbiol. 108, 105–111. https://doi.org/10.1007/bf00425099 (1976).

CAS  Article  PubMed  Google Scholar 

Watson, S. W., Graham, L. B., Remsen, C. C. & Valois, F. W. A lobular, ammonia-oxidizing bacterium, Nitrosolobus multiformis nov. gen. nov. sp. Archiv fur Mikrobiologie 76, 183–203. https://doi.org/10.1007/bf00409115 (1971).

CAS  Article  PubMed  Google Scholar 

Hiorns, W. D. et al. Amplification of 16S ribosomal RNA genes of autotrophic ammonia-oxidizing bacteria demonstrates the ubiquity of nitrosospiras in the environment. Microbiology 141(Pt 11), 2793–2800. https://doi.org/10.1099/13500872-141-11-2793 (1995).

Article  PubMed  Google Scholar 

Hastings, R. C. et al. Direct molecular biological analysis of ammonia oxidising bacteria populations in cultivated soil plots treated with swine manure. FEMS Microbiol. Ecol. 23, 45–54. https://doi.org/10.1111/j.1574-6941.1997.tb00390.x (1997).

CAS  Article  Google Scholar 

Ceccherini, M. T. et al. Effects of swine manure on autotrophic ammonia-oxidizing bacteria in soil microcosms. Appl. Soil Ecol. 7, 149–157 (1998).

Article  Google Scholar 

Martikainen, P. J. & Nurmiaho-Lassila, E.-L. Nitrosospira, an important ammonium-oxidizing bacterium in fertilized coniferous forest soil. Can. J. Microbiol. 31, 190–197. https://doi.org/10.1139/m85-037 (1985).

CAS  Article  Google Scholar 

Kowalchuk, G. A., Stienstra, A. W., Heilig, G. H., Stephen, J. R. & Woldendorp, J. W. Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ. Microbiol. 2, 99–110 (2000).

CAS  Article  Google Scholar 

Speksnijder, A. G., Kowalchuk, G. A., Roest, K. & Laanbroek, H. J. Recovery of a Nitrosomonas-like 16S rDNA sequence group from freshwater habitats. Syst. Appl. Microbiol. 21, 321–330. https://doi.org/10.1016/s0723-2020(98)80040-4 (1998).

CAS  Article  PubMed  Google Scholar 

Whitby, C. B., Saunders, J. R., Pickup, R. W. & McCarthy, A. J. A comparison of ammonia-oxidiser populations in eutrophic and oligotrophic basins of a large freshwater lake. Antonie Van Leeuwenhoek 79, 179–188. https://doi.org/10.1023/A:1010202211368 (2001).

CAS  Article  PubMed  Google Scholar 

Burrell, P. C., Phalen, C. M. & Hovanec, T. A. Identification of Bacteria Responsible For Ammonia Oxidation In Freshwater Aquaria. Appl. Environ. Microbiol. 67, 5791–5800. https://doi.org/10.1128/aem.67.12.5791-5800.2001 (2001).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Spieck, E., Meincke, M. & Bock, E. Taxonomic diversity of Nitrosovibrio strains isolated from building sandstones. FEMS Microbiol. Ecol. 11, 21–26. https://doi.org/10.1111/j.1574-6968.1992.tb05791.x (1992).

Article  Google Scholar 

Nugroho, R. A., Roling, W. F., Laverman, A. M., Zoomer, H. R. & Verhoef, H. A. Presence of Nitrosospira cluster 2 bacteria corresponds to N transformation rates in nine acid Scots pine forest soils. FEMS Microbiol. Ecol. 53, 473–481. https://doi.org/10.1016/j.femsec.2005.02.002 (2005).

CAS  Article  PubMed  Google Scholar 

Stephen, J. R., McCaig, A. E., Smith, Z., Prosser, J. I. & Embley, T. M. Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 62, 4147–4154 (1996).

CAS  Article  Google Scholar 

Phillips, C. J., Smith, Z., Embley, T. M. & Prosser, J. I. Phylogenetic differences between particle-associated and planktonic ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in the Northwestern Mediterranean Sea. Appl. Environ. Microbiol. 65, 779–786 (1999).

CAS  Article  Google Scholar 

Bano, N. & Hollibaugh, J. T. Diversity and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in the Arctic Ocean. Appl. Environ. Microbiol. 66, 1960–1969 (2000).

CAS  Article  Google Scholar 

McCaig, A. E., Embley, T. M. & Prosser, J. I. Molecular analysis of enrichment cultures of marine ammonia oxidisers. FEMS Microbiol. Lett. 120, 363–367 (1994).

CAS  Article  Google Scholar 

Nicolaisen, M. H. & Ramsing, N. B. Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J. Microbiol. Methods 50, 189–203 (2002).

CAS  Article  Google Scholar 

Freitag, T. E., Chang, L. & Prosser, J. I. Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient. Environ. Microbiol. 8, 684–696. https://doi.org/10.1111/j.1462-2920.2005.00947.x (2006).

CAS  Article  PubMed  Google Scholar 

Wankel, S. D., Mosier, A. C., Hansel, C. M., Paytan, A. & Francis, C. A. Spatial variability in nitrification rates and ammonia-oxidizing microbial communities in the agriculturally impacted Elkhorn Slough estuary, California. Appl. Environ. Microbiol. 77, 269–280. https://doi.org/10.1128/aem.01318-10 (2011).

CAS  Article  PubMed  Google Scholar 

Jacob, J., Sanders, T. & Dähnke, K. Nitrite consumption and associated isotope changes during a river flood event. Biogeosciences 13, 5649–5659. https://doi.org/10.5194/bg-13-5649-2016 (2016).

ADS  CAS  Article  Google Scholar 

Voynova, Y. G., Brix, H., Petersen, W., Weigelt-Krenz, S. & Scharfe, M. Extreme flood impact on estuarine and coastal biogeochemistry: The 2013 Elbe flood. Biogeosciences 14, 541–557. https://doi.org/10.5194/bg-14-541-2017 (2017).

ADS  CAS  Article  Google Scholar 

Pommerening-Röser, A., Rath, G. & Koops, H. P. Phylogenetic diversity within the genus Nitrosomonas. Syst. Appl. Microbiol. 19, 344–351. https://doi.org/10.1016/S0723-2020(96)80061-0 (1996).

Article  Google Scholar 

Nacke, H. et al. Links between seawater flooding, soil ammonia oxidiser communities and their response to changes in salinity. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fix144 (2017).

Article  PubMed  Google Scholar 

Laanbroek, H. J., Keijzer, R. M., Verhoeven, J. T. & Whigham, D. F. The distribution of ammonia-oxidizing betaproteobacteria in stands of black mangroves (Avicennia germinans). Front. Microbiol. 3, 153. https://doi.org/10.3389/fmicb.2012.00153 (2012).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Juretschko, S. et al. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 64, 3042–3051 (1998).

CAS  Article  Google Scholar 

Daims, H. et al. Nitrification in sequencing biofilm batch reactors: Lessons from molecular approaches. Water Sci. Technol. 43, 9–18 (2001).

ADS  CAS  Article  Google Scholar