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Monthly distribution of ammonia-oxidizing microbes in a tropical bay

  • Microbial Ecology and Environmental Microbiology
  • Published:
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Abstract

Ammonia oxidation, performed by ammonia-oxidizing archaea (AOA) and bacteria (AOB), plays a critical role in the cycle of nitrogen in the ocean. For now, environmental variables controlling distribution of ammonia-oxidizing microbes are still largely unknown in oceanic environments. In this study, we used real-time quantitative PCR and high-throughput sequencing methods to investigate the abundance and diversity of AOA and AOB from sediment and water in Zhanjiang Bay. Phylogenic analysis revealed that the majority of AOA amoA sequences in water and sediment were affiliated with the genus Nitrosopumilus, whereas the Nitrosotalea cluster was only detected with low abundance in water. Nitrosomonas and Nitrosospira dominated AOB amoA sequences in water and sediment, respectively. The amoA copy numbers of both AOA and AOB varied significantly with month for both sediment and water. When water and sediment temperature dropped to 17–20°C in December and February, respectively, the copy number of AOB amoA genes increased markedly and was much higher than for AOA amoA genes. Also, AOA abundance in water peaked in December when water temperature was lowest (17–20°C). Stepwise multiple regression analyses revealed that temperature was the most key factor driving monthly changes of AOA or AOB abundance. It is inferred that low water temperature may inhibit growth of phytoplankton and other microbes and so reduce competition for a common substrate, ammonium.

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References

  • Amato, K.R., Yeoman, C.J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Gaskins, H.R., Stumpf, R.M., Yildirim, S., Torralba, M., et al. 2013. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344–1353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amin, S.A., Moffett, J.W., Martens-Habbena, W., Jacquot, J.E., Han, Y., Devol, A., Ingalls, A.E., Stahl, D.A., and Armbrust, E.V. 2013. Copper requirements of the ammonia-oxidizing archaeon Nitrosopumilus maritimus SCM1 and implications for nitrification in the marine environment. Limnol. Oceangr. 58, 2037–2045.

    Article  CAS  Google Scholar 

  • Auguet, J.C. and Casamayor, E.O. 2013. Partitioning of Thaumarchaeota populations along environmental gradients in high mountain lakes. FEMS Microbiol. Ecol. 84, 154–164.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Beman, J.M. and Francis, C.A. 2006. Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico. Appl. Environ. Microbiol. 72, 7767–7777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolger, A.M., Lohse, M., and Usadel, B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao, H., Hong, Y., Li, M., and Gu, J.D. 2011a. Diversity and abundance of ammonia-oxidizing prokaryotes in sediments from the coastal Pearl River estuary to the South China Sea. Antonie van Leeuwenhoek 100, 545–556.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao, H., Hong, Y., Li, M., and Gu, J.D. 2011b. Phylogenetic diversity and ecological pattern of ammonia-oxidizing archaea in the surface sediments of the western Pacific. Microb. Ecol. 62, 813.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao, H., Zhang, W., Wang, Y., and Qian, P.Y. 2015. Microbial community changes along the active seepage site of one cold seep in the Red Sea. Front. Microbiol. 6, 739.

    PubMed  PubMed Central  Google Scholar 

  • Chen, Y., Zhen, Y., He, H., Lu, X., Mi, T., and Yu, Z. 2014. Diversity, abundance, and spatial distribution of ammonia-oxidizing β-proteobacteria in sediments from Changjiang Estuary and its adjacent area in East China Sea. Microb. Ecol. 67, 788–803.

    Article  CAS  PubMed  Google Scholar 

  • Christman, G.D., Cottrell, M.T., Popp, B.N., Gier, E., and Kirchman, D.L. 2011. Abundance, diversity, and activity of ammonia-axidizing prokaryotes in the coastal Arctic Ocean in summer and winter. Appl. Environ. Microbiol. 77, 2026–2034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daims, H., Lebedeva, E.V., Pjevac, P., Han, P., Herbold, C., Albertsen, M., Jehmlich, N., Palatinszky, M., Vierheilig, J., Bulaev, A., et al. 2015. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dang, H., Li, J., Chen, R., Wang, L., Guo, L., Zhang, Z., and Klotz, M.G. 2010. Diversity, abundance, and spatial distribution of sediment ammonia-oxidizing Betaproteobacteria in response to environmental gradients and coastal eutrophication in Jiaozhou Bay, China. Appl. Environ. Microbiol. 76, 4691–4702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dang, H., Zhou, H., Yang, J., Ge, H., Jiao, N.Z., Luan, X.W., Zhang, C., and Klotz, M.G. 2013. Thaumarchaeotal signature gene distribution in sediments of the northern South China Sea: an indicator of the metabolic intersection of the marine carbon, nitrogen, and phosphorus cycles? Appl. Environ. Microbiol. 79, 2137–2147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edger, R.C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998.

    Article  CAS  Google Scholar 

  • Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaudette, H.E., Flight, W.R., and Toner, L. 1974. An inexpensive titration method for the determination of organic carbon in recent sediments. J. Sediment. Res. 44, 249–253.

    CAS  Google Scholar 

  • Horak, R.E.A., Qin, W., Schauer, A.J., Armbrust, E.V., Ingalls, A.E., Moffett, J.W., Stahl, D.A., and Devol, A.H. 2013. Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by Archaea. ISME J. 7, 2023–2033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou, J., Song, C., Cao, X., and Zhou, Y. 2013. Shifts between ammonia-oxidizing bacteria and archaea in relation to nitrification potential across trophic gradients in two large Chinese lakes (Lake Taihu and Lake Chaohu). Water Res. 47, 2285–2296.

    Article  CAS  PubMed  Google Scholar 

  • Hou, M., Xiong, J., Wang, K., Ye, X.S., Ye, R., Wang, Q., Hu, C., and Zhang, D. 2014. Communities of sediment ammonia-oxidizing bacteria along a coastal pollution gradient in the East China Sea. Mar. Pollut. Bull. 86, 147–153.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, H., Dong, H., Yu, B., Lv, G., Deng, S., Berzins, N., and Dai, M. 2009. Diversity and abundance of ammonia-oxidizing archaea and bacteria in Qinghai Lake, northwestern China. Geomicrobiol. J. 26, 199–211.

    Article  CAS  Google Scholar 

  • Jin, T., Zhang, T., Ye, L., Lee, O.O., Wong, Y.H., and Qian, P.Y. 2011. Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River Estuary, China. Appl. Microbiol. Biotechnol. 90, 1137–1145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, R., Morita, R., Koops, H.P., and Watson, S.W. 1988. A new marine ammonium-oxidizing bacterium, Nitrosomonas cryotolerans sp. nov. Can. J. Microbiol. 34, 1122–1128.

    Article  CAS  Google Scholar 

  • Könneke, M., Bernhard, A.E., de la Torre, J.R., Walker, C.B., Waterbury, J.B., and Stahl, D.A. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546.

    Article  PubMed  CAS  Google Scholar 

  • Li, M., Cao, H., Hong, Y., and Gu, J.D. 2011. Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl. Microbiol. Biotechnol. 89, 1243–1254.

    Article  CAS  PubMed  Google Scholar 

  • Li, M., Wei, G., Shi, W., Sun, Z., Li, H., Wang, X., and Gao, Z. 2018. Distinct distribution patterns of ammonia-oxidizing archaea and bacteria in sediment and water column of the Yellow River estuary. Sci. Rep. 8, 1584.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, S., Shen, L., Lou, L., Tian, G., Zheng, P., and Hu, B. 2013. Spatial distribution and factors shaping the niche segregation of ammonia-oxidizing microorganisms in the Qiantang River, China. Appl. Environ. Microbiol. 79, 4065–4071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Q., Tolar, B.B., Ross, M.J., Cheek, J.B., Sweeney, C.M., Wallsgrove, N.J., Popp, B.N., and Hollibaugh, J.T. 2018. Light and temperature control the seasonal distribution of thaumarchaeota in the South Atlantic bight. ISME J. 12, 1473–1485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lozupone, C. and Knight, R. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, Z.H., Xu, W., Li, M., Gu, J.D., and Zhong, T.H. 2015. Spatial distribution and abundance of ammonia-oxidizing microorganisms in deep-sea sediments of the Pacific Ocean. Antonie van Leeuwenhoek 108, 329–342.

    Article  CAS  PubMed  Google Scholar 

  • Magoč, T. and Salzberg, S.L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mantoura, R.F.C. and Woodward, E.M.S. 1983. Optimization of the indophenol blue method for the automated determination of ammonia in estuarine waters. Estuar. Coast. Shelf Sci. 17, 219–224.

    Article  CAS  Google Scholar 

  • Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, J.R., and Stahl, D.A. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461, 976–979.

    Article  CAS  PubMed  Google Scholar 

  • Mosier, A.C. and Francis, C.A. 2008. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ. Microbiol. 10, 3002–3016.

    Article  CAS  PubMed  Google Scholar 

  • Oishi, R., Tada, C., Asano, R., Yamamoto, N., Suyama, Y., and Nakai, Y. 2012. Growth of ammonia-oxidizing archaea and bacteria in cattle manure compost under various temperatures and ammonia concentrations. Microb. Ecol. 63, 787–793.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pereira e Silva, M.C., Poly, F., Guillaumaud, N., van Elsas, J., and Falcão Salles, J. 2012. Fluctuations in ammonia oxidizing communities across agricultural soils are driven by soil structure and pH. Front. Microbiol. 3, 77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pett-Ridge, J., Petersen, D.G., Nuccio, E., and Firestone, M.K. 2013. Influence of oxic/anoxic fluctuations on ammonia oxidizers and nitrification potential in a wet tropical soil. FEMS Microbiol. Ecol. 85, 179–194.

    Article  PubMed  Google Scholar 

  • Purkhold, U., Pommerening-Röser, A., Juretschko, S., Schmid, M.C., Koops, H.P., and Wagner, M. 2000. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl. Environ. Microbiol. 66, 5368–5382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin, W., Amin, S.A., Martens-Habbena, W., Walker, C.B., Urakawa, H., Devol, A.H., Ingalls, A.E., Moffett, J.W., Armbrust, E.V., and Stahl, D.A. 2014. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc. Natl. Acad. Sci. USA 111, 12504–12509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rotthauwe, J.H., Witzel, K.P., and Liesack, W. 1997. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soon, Y.K. and Abboud, S. 1991. A comparison of some methods for soil organic carbon determination. Commun. Soil Sci. Plant Anal. 22, 943–954.

    Article  CAS  Google Scholar 

  • Stewart, B.M. and Elliott, P.A.W. 1996. Systematic salt effects in the automated determination of nutrients in seawater. Water Res. 30, 869–874.

    Article  CAS  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tourna, M., Freitag, T.E., Nicol, G.W., and Prosser, J.I. 2008. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10, 1357–1364.

    Article  CAS  PubMed  Google Scholar 

  • Urakawa, H., Martens-Habbena, W., Huguet, C., de la Torre, J.R., Ingalls, A.E., Devol, A.H., and Stahl, D.A. 2014. Ammonia availability shapes the seasonal distribution and activity of archaeal and bacterial ammonia oxidizers in the Puget Sound estuary. Limnol. Oceanogr. 59, 1321–1335.

    Article  CAS  Google Scholar 

  • van Kessel, M.A.H.J., Speth, D.R., Albertsen, M., Nielsen, P.H., Op den Camp, H.J.M., Kartal, B., Jetten, M.S.M., and Lücker, S. 2015. Complete nitrification by a single microorganism. Nature 528, 555–559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, J., Kan, J., Zhang, X., Xia, Z., Zhang, X., Qian, G., Miao, Y., Leng, X., and Sun, J. 2017. Archaea dominate the ammonia-oxidizing community in deep-sea sediments of the eastern Indian Ocean-from the Equator to the Bay of Bengal. Front. Microbiol. 8, 415.

    PubMed  PubMed Central  Google Scholar 

  • Wu, L., Han, C., Zhu, G., and Zhong, W. 2019. Responses of active ammonia oxidizers and nitrification activity in eutrophic lake sediments to nitrogen and temperature. Appl. Environ. Microbiol. 85, e00258–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, T., Li, M., Niu, M., Fan, X., Liang, W., and Wang, F. 2018. Difference of nitrogen-cycling microbes between shallow bay and deep-sea sediments in the South China Sea. Appl. Microbiol. Biotechnol. 102, 447–459.

    Article  CAS  PubMed  Google Scholar 

  • Yu, S., Yao, P., Liu, J., Zhao, B., Zhang, G., Zhao, M., Yu, Z., and Zhang, X.H. 2016. Diversity, abundance, and niche differentiation of ammonia-oxidizing prokaryotes in mud deposits of the Eastern China marginal seas. Front. Microbiol. 7, 137.

    PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Chen, L., Sun, R., Dai, T., Tian, J., Zheng, W., and Wen, D. 2016. Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants’ receiving area in Hangzhou Bay. Appl. Microbiol. Biotechnol. 100, 6035–6045.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, Y., Hou, L., Liu, M., Lu, M., Zhao, H., Yin, G., and Zhou, J. 2013. Diversity, abundance, and activity of ammonia-oxidizing bacteria and archaea in Chongming eastern intertidal sediments. Appl. Microbiol. Biotechnol. 97, 8351–8363.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, L., Wang, S., Zou, Y., Xia, C., and Zhu, G. 2015. Species, abundance and function of ammonia-oxidizing archaea in inland waters across China. Sci. Rep. 5, 15969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was funded by the National Natural Science Foundation of China (41971125 and 41725002), the Guangdong Natural Science Foundation (2018A030313164) and the Innovation Study Project of East China Normal University. The funders had no role in the study design, data collection and analysis, and interpretation of data and in manuscript preparation. We thank Qingmei Zhu and Fajin Chen for providing partial nutrient data in water from Zhanjiang Bay.

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Authors and Affiliations

  1. State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai, 200062, P. R. China

    Hong-Po Dong & Li-Jun Hou

  2. School of Ocean and Meteorology, Guangdong Ocean University, Zhanjiang, 524088, P. R. China

    Tie-Qiang Mao, Yan-Qun Li & Wen-Na Yang

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  1. Tie-Qiang Mao
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  2. Yan-Qun Li
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Correspondence to Hong-Po Dong.

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The authors declare that they have no competing interests.

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request. All raw sequence reads in this study were deposited in the NCBI Sequence Read Archive (SRA) under accession number PRJNA545841 with the individual accession numbers for each BioSample: SAMN11935587- SAMN11935604.

Author Contributions

HPD and YQL conceived and designed the study and WNY, QHH and TQM performed experiments and analyzed data. HPD wrote the manuscript. All authors have read and approved the manuscript.

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We declare that sample collection has been approved by local government.

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Mao, TQ., Li, YQ., Dong, HP. et al. Monthly distribution of ammonia-oxidizing microbes in a tropical bay. J Microbiol. 59, 10–19 (2021). https://doi.org/10.1007/s12275-021-0287-5

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