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Communities of ammonia oxidizers at different stages of Spartina alterniflora invasion in salt marshes of Yangtze River estuary

  • Microbial Ecology and Environmental Microbiology
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Abstract

Spartina alterniflora, an aggressive invasive plant species at the estuarine wetlands of China’s coasts, has become a major threat to the natural ecosystems. To understand its potential influence on nitrification processes, the community structures and abundance of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) were investigated using 454-pyrosequencing and quantitative real-time PCR (qPCR) in S. alterniflora invading salt marsh sediments at the Yangtze River estuary in Chongming island, Shanghai, China. Copy numbers of archaeal and bacterial ammonia monooxygenase subunit A (amoA) genes did not show accordant shifts with S. alterniflora invasion in the two sampling sites. However, the copy numbers of archaeal amoA gene were higher in summer than in spring. Phylogenetic analysis indicated that more than 90% of the archaeal and 92% of the bacterial amoA gene sequences were closely related to marine group I.1a and the clusters 13 and 15 in Nitrosospira lineage, respectively. The effect of different seasons (spring and summer) was important for the abundance variation of AOA, while different stages of S. alterniflora invasion did not show significant effect for both AOA and AOB. Variation of AOA community was significantly related to total carbon (TC) and sulfate concentration (P < 0.05), whereas the AOB community was significantly related to sulfate concentration, total nitrogen (TN), TC and pH (P < 0.05). In conclusion, the abundance and diversity of ammonia oxidizing microbial communities were not strongly affected by S. alterniflora invasion.

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References

  • Abell, G.C.J., Revill, A.T., Smith, C., Bissett, A.P., Volkman, J.K., and Robert, S.S. 2009. Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J. 4, 286–300.

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bai, S., Li, J., He, Z., Van Nostrand, J.D., Tian, Y., Lin, G., Zhou, J., and Zheng, T. 2013. Geochip-based analysis of the functional gene diversity and metabolic potential of soil microbial communities of mangroves. Appl. Microbiol. Biotechnol. 15, 1–14.

    Google Scholar 

  • Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., and Vivanco, J.M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233–266.

    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: Bahia del Tobari, Mexico. Appl. Environ. Microbiol. 72, 7767–7777.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beman, J.M., Sachdeva, R., and Fuhrman, J.A. 2010. Population ecology of nitrifying archaea and bacteria in the southern california bight. Environ. Microbiol. 12, 1282–1292.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bernhard, A.E., Landry, Z.C., Blevins, A., José, R., Giblin, A.E., and Stahl, D.A. 2010. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl. Environ. Microbiol. 76, 1285–1289.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berry, D., Mahfoudh, K.B., Wagner, M., and Loy, A. 2011. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol. 77, 7846–7849.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. 2008. Mesophilic crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245–252.

    Article  CAS  PubMed  Google Scholar 

  • Caffrey, J.M., Bano, N., Kalanetra, K., and Hollibaugh, J.T. 2007. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J. 1, 660–662.

    Article  PubMed  Google Scholar 

  • Cheng, X., Peng, R., Chen, J., Luo, Y., Zhang, Q., An, S., Chen, J., and Li, B. 2007. CH4 and N2O emissions from Spartina alterniflora and Phragmites australis in experimental mesocosms. Chemosphere 68, 420–427.

    Article  CAS  PubMed  Google Scholar 

  • Craft, C., Clough, J., Ehman, J., Joye, S., Park, R., Pennings, S., Guo, H., and Machmuller, M. 2008. Forecasting the effects of accelerated sealevel rise on tidal marsh ecosystem services. Front. Ecol. Environ. 7, 73–78.

    Article  Google Scholar 

  • Damsté, J.S.S., Rijpstra, W.I.C., Hopmans, E.C., Jung, M.Y., Kim, J.G., Rhee, S.K., Stieglmeier, M., and Schleper, C. 2012. Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I.1a and I.1b Thaumarchaeota in soil. Appl. Environ. Microbiol. 78, 6866–6874.

    Article  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Fan, F., Yang, Q., Li, Z., Wei, D., Cui, X., and Liang, Y. 2011. Impacts of organic and inorganic fertilizers on nitrification in a cold climate soil are linked to the bacterial ammonia oxidizer community. Microb. Ecol. 62, 982–990.

    Article  PubMed  Google Scholar 

  • Fenchel, T. 2002. Microbial behavior in a heterogeneous world. Science 296, 1068–1071.

    Article  CAS  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Haichar, F.Z., Marol, C., Berge, O., Rangel-Castro, J.I., Prosser, J.I., Balesdent, J., Heulin, T., and Achouak, W. 2008. Plant host habitat and root exudates shape soil bacterial community structure. ISME J. 2, 1221–1230.

    Article  CAS  PubMed  Google Scholar 

  • Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.

    CAS  Google Scholar 

  • Hansel, C.M., Fendorf, S., Jardine, P.M., and Francis, C.A. 2008. Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl. Environ. Microbiol. 74, 1620–1633.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hatzenpichler, R., Lebedeva, E.V., Spieck, E., Stoecker, K., Richter, A., Daims, H., and Wagner, M. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 105, 2134–2139.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayashi, T., Kaneko, R., Tanahashi, M., and Naganuma, T. 2007. Molecular diversity of the genes encoding ammonia monooxygenase and particulate methane monooxygenase from deep-sea sediments. Res. J. Microbiol. 2, 530–537.

    Article  CAS  Google Scholar 

  • Hollibaugh, J.T., Gifford, S.M., Moran, M.A., Ross, M.J., Sharma, S., and Tolar, B.B. 2014. Seasonal variation in the metratranscriptomes of a Thaumarchaeota population from SE USA coastal waters. ISME J. 8, 685–698.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hou, L.J., Liu, M., Jiang, H.Y., Xu, S.Y., Ou, D.N., Liu, Q.M., and Zhang, B.L. 2003. Ammonium adsorption by tidal flat surface sediments from the Yangtze estuary. Environ. Geol. 45, 72–78.

    Article  CAS  Google Scholar 

  • Hu, Z., Meng, H., Shi, J.H., Bu, N.S., Fang, C.M., and Quan, Z.X. 2014. Community size and composition of ammonia oxidizers and denitrifiers in an alluvial intertidal wetland ecosystem. Front. Microbiol. 5, 371.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ingalls, A.E., Shah, S.R., Hansman, R.L., Aluwihare, L.I., Santos, G.M., Druffel, E.R., and Pearson, A. 2006. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl. Acad. Sci. USA 103, 6442–6447.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jia, Z. and Conrad, R. 2009. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11, 1658–1671.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, L.F., Luo, Y.Q., Chen, J.K., and Li, B. 2009. Ecophysiological characteristics of invasive Spartina alterniflora and native species in salt marshes of Yangtze River estuary, China. Estuar. Coast. Shelf. Sci. 81, 74–82.

    Article  Google Scholar 

  • Kim, J., Jung, M., Lee, K., Kim, D., Ko, S., Lee, J., and Rhee, S. 2014. The archaea community associated with lava-formed Gotjawal forest soil in Jeju, Korea. J. Agr. Chem. Environ. 3, 96–102.

    Google Scholar 

  • Kim, J., Jung, M., Lee, K., Kim, D., Ko, S., Lee, J., and Rhee, S. 2014. The Archaea community associated with lava-formed Gotjawal forest soil in Jeju, Korea. J. Agr. Chem. Environ. 3, 96-102.

    Google Scholar 

  • Kim, J.G., Jung, M.Y., Park, S.J., Rijpstra, W.I.C., Sinninghe Damsté, J.S., Madsen, E.L., Min, D., Kim, J.S., Kim, G.J., and Rhee, S.K. 2012. Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ. Microbiol. 14, 1528–1543.

    Article  CAS  PubMed  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  Google Scholar 

  • Kowalchuk, G.A. and Stephen, J.R. 2001. Ammonia-oxidizing bacteria: A model for molecular microbial ecology. Annu. Rev. Microbiol. 55, 485–529.

    Article  CAS  PubMed  Google Scholar 

  • Lage, M.D., Reed, H.E., Weihe, C., Crain, C.M., and Martiny, J.B. 2010. Nitrogen and phosphorus enrichment alter the composition of ammonia-oxidizing bacteria in salt marsh sediments. ISME J. 4, 933–944.

    Article  CAS  PubMed  Google Scholar 

  • Larkin, M.A., Blackshields, G., Brown, N., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., and Lopez, R. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23, 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  • Leininger, S., Urich, T., SchloteS, M., Schwark, L., Qi, J., Nicol, G., Prosser, J., Schuster, S., and Schleper, C. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809.

    Article  CAS  PubMed  Google Scholar 

  • Li, X.R., Xiao, Y.P., Ren, W.W., Liu, Z.F., Shi, J.H., and Quan, Z.X. 2012. Abundance and composition of ammonia-oxidizing bacteria and archaea in different types of soil in the Yangtze river estuary. J. Zhejiang. Univ. Sci. B. 13, 769–782.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liao, C., Luo, Y., Jiang, L., Zhou, X., Wu, X., Fang, C., Chen, J., and Li, B. 2007. Invasion of Spartina alterniflora enhanced ecosystem carbon and nitrogen stocks in the Yangtze estuary, China. Ecosystems 10, 1351–1361.

    Article  CAS  Google Scholar 

  • Mincer, T.J., Church, M.J., Taylor, L.T., Preston, C., Karl, D.M., and DeLong, E.F. 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in monterey bay and the Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9, 1162–1175.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  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 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Page, H.M., Lastra, M., Rodil, I.F., Briones, M.J.I., and Garrido, J. 2010. Effects of non-native Spartina patens on plant and sediment organic matter carbon incorporation into the local invertebrate community. Biol. Invasions 12, 3825–3838.

    Article  Google Scholar 

  • Parameswaran, P., Jalili, R., Tao, L., Shokralla, S., Gharizadeh, B., Ronaghi, M., and Fire, A.Z. 2007. A pyrosequencing-tailored nucleotide barcode design unveils opportunities for large-scale sample multiplexing. Nucleic Acids Res. 35, e130.

    Article  Google Scholar 

  • Park, B.J., Park, S.J., Yoon, D.N., Schouten, S., Sinninghe Damsté, J.S., and Rhee, S.K. 2010. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl. Environ. Microbiol. 76, 7575–7587.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pester, M., Schleper, C., and Wagner, M. 2011. The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300–306.

    Article  PubMed Central  CAS  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Quan, W., Han, J., Shen, A., Ping, X., Qian, P., Li, C., Shi, L., and Chen, Y. 2007. Uptake and distribution of N, P and heavy metals in three dominant salt marsh macrophytes from Yangtze River estuary, China. Mar. Environ. Res. 64, 21–37.

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team. 2004. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (http://www.r-project.org).

    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.

    PubMed Central  CAS  PubMed  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., and Robinson, C.J. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Seyler, L.M., McGuinness, L.M., and Kerkhof, L.J. 2014. Crenarchaeal heterotrophy in salt marsh sediments. ISME J. 8, 1534–1543.

    Article  CAS  PubMed  Google Scholar 

  • Szukics, U., Abell, G.C., Hödl, V., Mitter, B., Sessitsch, A., Hackl, E., and Zechmeister-Boltenstern, S. 2010. Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol. Ecol. 72, 395–406.

    Article  PubMed Central  CAS  PubMed  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  PubMed Central  CAS  PubMed  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 

  • Treusch, A.H., Leininger, S., Kletzin, A., Schuster, S.C., Klenk, H.P., and Schleper, C. 2005. Novel genes for nitrite reductase and amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling. Environ. Microbiol. 7, 1985–1995.

    Article  CAS  PubMed  Google Scholar 

  • Turner, R.E. 1993. Carbon, nitrogen, and phosphorus leaching rates from Spartina alterniflora salt marshes. Mar. Ecol. Prog. Ser. 92, 135–140.

    Article  CAS  Google Scholar 

  • Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., and Nelson, W. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Q., Quensen, J.F., Fish, J.A., Lee, T.K., Sun, Y., Tiedje, J.M., and Cole, J.R. 2013. Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. MBio 4, E00592–00513.

    Google Scholar 

  • Wankel, S.D., Mosier, A.C., Hansel, C.M., Paytan, A., and Francis, C.A. 2011. Spatial variability in nitrification rates and ammonia-oxidizing microbial communities in the agriculturally impacted Elkhorn Slough estuary, California. Appl. Environ. Microbiol. 77, 269–280.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Williams, S.L. and Grosholz, E.D. 2008. The invasive species challenge in estuarine and coastal environments: Marrying management and science. Estuar. Coast 31, 3–20.

    Article  Google Scholar 

  • Yao, H., Campbell, C.D., Chapman, S.J., Freitag, T.E., Nicol, G.W., and Singh, B.K. 2013. Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environ. Microbiol. 15, 2545–2556.

    Article  CAS  PubMed  Google Scholar 

  • Zeleke, J., Sheng, Q., Wang, J.G., Huang, M.Y., Xia, F., Wu, J.H., and Quan, Z.X. 2013. Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Front Microbiol. 4, 243.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang, Q.F., Peng, J.J., Chen, Q., Li, X.F., Xu, C.Y., Yin, H.B., and Yu, S. 2011. Impacts of Spartina alterniflora invasion on abundance and composition of ammonia oxidizers in estuarine sediment. J. Soils Sediments. 11, 1020–1031.

    Article  Google Scholar 

  • Zhang, L.M., Wang, M., Prosser, J.I., Zheng, Y.M., and He, J.Z. 2009. Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol. Ecol. 70, 208–217.

    Article  CAS  Google Scholar 

  • Zheng, Y., Hou, L., Liu, M., Lu, M., Zhao, H., Yin, G., and Zhou, J. 2012. Diversity, abundance, and activity of ammonia-oxidizing bacteria and archaea in Chongming eastern intertidal sediments. Appl. Microbiol. Biotechnol. 97, 8351–8363.

    Article  PubMed  Google Scholar 

  • Zheng, Y., Hou, L., Newell, S., Liu, M., Zhou, J., Zhao, H., You, L., and Cheng, X. 2014. Community dynamics and activity of ammonia-oxidizing prokaryotes in intertidal sediments of the Yangtze estuary. Appl. Environ. Microbiol. 80, 408–419.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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  1. Department of Microbiology and Microbial Engineering, School of Life Sciences, Fudan University, Shanghai, China

    Fei Xia, Jemaneh Zeleke & Zhe-Xue Quan

  2. Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Department of Ecology and Evolutionary Biology, Fudan University, Shanghai, China

    Fei Xia, Qiang Sheng & Ji-Hua Wu

  3. Department of Biology, College of Natural and Computational Sciences, Wolaita Sodo University, Sodo, Ethiopia

    Jemaneh Zeleke

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Xia, F., Zeleke, J., Sheng, Q. et al. Communities of ammonia oxidizers at different stages of Spartina alterniflora invasion in salt marshes of Yangtze River estuary. J Microbiol. 53, 311–320 (2015). https://doi.org/10.1007/s12275-015-4660-0

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