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Niche differentiation of comammox Nitrospira and canonical nitrifiers in riparian wetland ecosystems around Taihu Lake

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
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Abstract

Purpose

Complete ammonia oxidation (comammox) overturned the traditional two-step nitrification theory. Newly discovered comammox Nitrospira and canonical nitrifiers (ammonia-oxidizing archaea and ammonia-oxidizing bacteria) collaboratively perform the oxidation of ammonia in ecosystems. However, the niche distribution of three ammonia oxidizers is controversial. In this study, we explored the distribution and diversity of comammox Nitrospira in riparian wetland ecosystems around Taihu Lake.

Materials and methods

Soil samples were collected from five habitats: wheat field, vegetable field, peach orchard, tea orchard, and small camphor forest. The abundances and diversity of comammox Nitrospira amoA gene were measured.

Results and discussion

The amoA gene abundance of comammox Nitrospira varied greatly, ranging from 1.83 × 105 to 8.35 × 107 copies/g. Temperature, total nitrogen, total carbon, and pH showed significant correlations with the amoA gene abundance of three ammonia oxidizers. High-throughput sequencing suggested that the community structure of comammox Nitrospira showed both spatial and temporal heterogeneity. Total carbon and pH could be the prime environmental factors causing the niche differentiation between comammox Nitrospira and canonical nitrifiers. Moisture content and NH4+ affected the community structure of comammox Nitrospira.

Conclusions

Three ammonia oxidizers distributed widely in riparian wetland ecosystems around Taihu Lake. Canonical nitrifiers were more competitive than comammox Nitrospira in most soil samples. Meanwhile, comammox Nitrospira seemed to prefer inhabiting oligotrophic conditions. Collectively, our study expands the general insights into the niche distribution of comammox Nitrospira and the driving environmental factors in riparian wetland ecosystems around Taihu Lake.

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Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  • Ai C, Zhang S, Zhang X, Guo D, Zhou W, Huang S (2018) Distinct responses of soil bacterial and fungal communities to changes in fertilization regime and crop rotation. Geoderma 319:156–166

    Article  CAS  Google Scholar 

  • Bach EM, Williams RJ, Hargreaves SK, Yang F, Hofmockel KS (2018) Greatest soil microbial diversity found in micro-habitats. Soil Biol Biochem 118:217–226

    Article  CAS  Google Scholar 

  • Bartelme RP, McLellan SL, Newton RJ (2017) Freshwater recirculating aquaculture system operations drive biofilter bacterial community shifts around a stable nitrifying consortium of ammonia-oxidizing archaea and comammox nitrospira. Front Microbiol 8:101

    Article  Google Scholar 

  • Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007

    Article  CAS  Google Scholar 

  • Costa E, Perez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14:213–219

    Article  CAS  Google Scholar 

  • Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509

    Article  CAS  Google Scholar 

  • Feng M, He Z-Y, Fan J, Ge A-H, Jin S, Lin Y, He J-Z (2022) Temperature has a strong impact on the abundance and community structure of comammox Nitrospira in an Ultisol. J Soils Sediments 22:2593–2603

    Article  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (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  Google Scholar 

  • Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 108:21206–21211

    Article  CAS  Google Scholar 

  • He S, Li Y, Mu H, Zhao Z, Wang J, Liu S, Sun Z, Zheng M (2021) Ammonium concentration determines differential growth of comammox and canonical ammonia-oxidizing prokaryotes in soil microcosms. Appl Soil Ecol 157:103766

    Article  Google Scholar 

  • Hu J, Zhao Y, Yao X, Wang J, Zheng P, Xi C, Hu B (2021) Dominance of comammox Nitrospira in soil nitrification. Sci Total Environ 780:146558

    Article  CAS  Google Scholar 

  • Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M (2017) Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549:269–272

    Article  CAS  Google Scholar 

  • Koch H, van Kessel MAHJ, Lücker S (2018) Complete nitrification: insights into the ecophysiology of comammox Nitrospira. Appl Microbiol Biotechnol 103:177–189

    Article  Google Scholar 

  • Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  Google Scholar 

  • Konneke M, Schubert DM, Brown PC, Hugler M, Standfest S, Schwander T, Schada von Borzyskowski L, Erb TJ, Stahl DA, Berg IA (2014) Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc Natl Acad Sci U S A 111:8239–8244

    Article  Google Scholar 

  • Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  CAS  Google Scholar 

  • Lawson CE, Lucker S (2018) Complete ammonia oxidation: an important control on nitrification in engineered ecosystems? Curr Opin Biotechnol 50:158–165

    Article  CAS  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  CAS  Google Scholar 

  • Li C, Hu H-W, Chen Q-L, Chen D, He J-Z (2020) Niche differentiation of clade A comammox Nitrospira and canonical ammonia oxidizers in selected forest soils. Soil Biol Biochem 149:107925

    Article  CAS  Google Scholar 

  • Li C, He Z-Y, Hu H-W, He J-Z (2022): Niche specialization of comammox Nitrospira in terrestrial ecosystems: Oligotrophic or copiotrophic? Crit Rev Environ Sci Technol 1–16

  • Liu Z, Zhang C, Wei Q, Zhang S, Quan Z, Li M (2020) Temperature and salinity drive comammox community composition in mangrove ecosystems across southeastern China. Sci Total Environ 742:140456

    Article  CAS  Google Scholar 

  • Lucker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Damste JS, Spieck E, Le Paslier D, Daims H (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci U S A 107:13479–13484

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Palomo A, Pedersen AG, Fowler SJ, Dechesne A, Sicheritz-Ponten T, Smets BF (2018) Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME J 12:1779–1793

    Article  Google Scholar 

  • Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel M, Daebeler A, Steinberger M, Jetten MSM, Lucker S, Wagner M, Daims H (2017) AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front Microbiol 8:1508

    Article  Google Scholar 

  • Rotthauwe JH, Witzel KP, 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  Google Scholar 

  • Sakoula D, Koch H, Frank J, Jetten MSM, van Kessel M, Lucker S (2021) Enrichment and physiological characterization of a novel comammox Nitrospira indicates ammonium inhibition of complete nitrification. ISME J 15:1010–1024

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Shao YH, Wu JH (2021) Comammox Nitrospira species dominate in an efficient partial nitrification-anammox bioreactor for treating ammonium at low loadings. Environ Sci Technol 55:2087–2098

    Article  CAS  Google Scholar 

  • Shi X, Hu H-W, Wang J, He J-Z, Zheng C, Wan X, Huang Z (2018) Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition. Soil Biol Biochem 126:114–122

    Article  CAS  Google Scholar 

  • Shi Y, Jiang Y, Wang S, Wang X, Zhu G (2020) Biogeographic distribution of comammox bacteria in diverse terrestrial habitats. Sci Total Environ 717:137257

    Article  CAS  Google Scholar 

  • Tiemann LK, Grandy AS, Atkinson EE, Marin-Spiotta E, McDaniel MD (2015) Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecol Lett 18:761–771

    Article  CAS  Google Scholar 

  • van Kessel M, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, Jetten MSM, Lucker S (2015) Complete nitrification by a single microorganism. Nature 528:555-+

  • Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc B Biol Sci 368:1621

    Article  Google Scholar 

  • Wang D-Q, Zhou C-H, Nie M, Gu J-D, Quan Z-X (2021a) Abundance and niche specificity of different types of complete ammonia oxidizers (comammox) in salt marshes covered by different plants. Sci Total Environ 768:1621

    Article  Google Scholar 

  • Wang M, Liu S, Wang F, Sun B, Zhou J, Yang Y (2015) Microbial responses to southward and northward Cambisol soil transplant. Microbiologyopen 4:931–940

    Article  Google Scholar 

  • Wang M, Huang G, Zhao Z, Dang C, Liu W, Zheng M (2018) Newly designed primer pair revealed dominant and diverse comammox amoA gene in full-scale wastewater treatment plants. Bioresour Technol 270:580–587

    Article  CAS  Google Scholar 

  • Wang Q, Wu Y, Guo D, Ma Y (2019a) Planting age of peach affects soil metal accumulation and distribution in soil profile. Environ Monit Assess 191:306

    Article  CAS  Google Scholar 

  • Wang S, Wang X, Jiang Y, Han C, Jetten MSM, Schwark L, Zhu G (2021b) Abundance and functional importance of complete ammonia oxidizers and other nitrifiers in a riparian ecosystem. Environ Sci Technol 55:4573–4584

    Article  CAS  Google Scholar 

  • Wang X, Wang S, Jiang Y, Zhou J, Han C, Zhu G (2020) Comammox bacterial abundance, activity, and contribution in agricultural rhizosphere soils. Sci Total Environ 727:138563

    Article  CAS  Google Scholar 

  • Wang Y, Ma L, Mao Y, Jiang X, Xia Y, Yu K, Li B, Zhang T (2017) Comammox in drinking water systems. Water Res 116:332–341

    Article  CAS  Google Scholar 

  • Wang Z, Cao Y, Zhu-Barker X, Nicol GW, Wright AL, Jia Z, Jiang X (2019b) Comammox Nitrospira clade B contributes to nitrification in soil. Soil Biol Biochem 135:392–395

    Article  CAS  Google Scholar 

  • Xu S, Wang B, Li Y, Jiang D, Zhou Y, Ding A, Zong Y, Ling X, Zhang S, Lu H (2020a) Ubiquity, diversity, and activity of comammox Nitrospira in agricultural soils. Sci Total Environ 706:135684

    Article  CAS  Google Scholar 

  • Xu Y, Liu G, Hua Y, Wan X, Hu J, Zhu D, Zhao J (2020b) The diversity of comammox bacteria and the effect of sewage discharge on their abundance in eutrophic lake sediments. J Soils Sediments 20:2495–2503

    Article  CAS  Google Scholar 

  • Yan P, Wu L, Wang D, Fu J, Shen C, Li X, Zhang L, Zhang L, Fan L, Wenyan H (2020) Soil acidification in Chinese tea plantations. Sci Total Environ 715:136963

    Article  CAS  Google Scholar 

  • Yang YC, Daims H, Liu Y, Herbold CW, Pjevac P, Lin JG, Li M, Gu JD (2020) Activity and metabolic versatility of complete ammonia oxidizers in full-scale wastewater treatment systems. Mbio 11:2

    Article  Google Scholar 

  • Yuan D, Zheng L, Tan Q, Wang X, Xing Y, Wang H, Wang S, Zhu G (2021) Comammox activity dominates nitrification process in the sediments of plateau wetland. Water Res 206:117774

    Article  CAS  Google Scholar 

  • Zeng J, Liu X, Song L, Lin X, Zhang H, Shen C, Chu H (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49

    Article  CAS  Google Scholar 

  • Zhang X, Dong W, Dai X, Schaeffer S, Yang F, Radosevich M, Xu L, Liu X, Sun X (2015) Responses of absolute and specific soil enzyme activities to long term additions of organic and mineral fertilizer. Sci Total Environ 536:59–67

    Article  CAS  Google Scholar 

  • Zhao Y, Hu J, Yang W, Wang J, Jia Z, Zheng P, Hu B (2021) The long-term effects of using nitrite and urea on the enrichment of comammox bacteria. Sci Total Environ 755:142580

    Article  CAS  Google Scholar 

  • Zheng M, Mu G, Zhang A, Wang J, Chang F, Niu J, Wang X, Gao T, Zhao Z (2022) Predominance of comammox bacteria among ammonia oxidizers under low dissolved oxygen condition. Chemosphere 308:136436

    Article  CAS  Google Scholar 

  • Zhu G, Wang X, Wang S, Yu L, Armanbek G, Yu J, Jiang L, Yuan D, Guo Z, Zhang H, Zheng L, Schwark L, Jetten MSM, Yadav AK, Zhu YG (2022) Towards a more labor-saving way in microbial ammonium oxidation: a review on complete ammonia oxidization (comammox). Sci Total Environ 829:154590

    Article  CAS  Google Scholar 

  • Zou W, Lang M, Zhang L, Liu B, Chen X (2022) Ammonia-oxidizing bacteria rather than ammonia-oxidizing archaea dominate nitrification in a nitrogen-fertilized calcareous soil. Sci Total Environ 811:151402

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (42177189).

Funding

National Natural Science Foundation of China, 42177189, Li Zhengkui

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Authors and Affiliations

  1. School of the Environment, Nanjing University, 163 Xianlin Avenue, 210023, Jiangsu, Nanjing, China

    Yanqing He, Yuecheng She, Xin Qi, Hui Zhang, Wei Wang & Zhengkui Li

  2. State Key Laboratory of Pollution Control and Resource Reuse, Nanjing University, 210023, Nanjing, China

    Yanqing He, Yuecheng She, Xin Qi, Hui Zhang, Wei Wang & Zhengkui Li

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  1. Yanqing He
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  2. Yuecheng She
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  3. Xin Qi
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Correspondence to Zhengkui Li.

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He, Y., She, Y., Qi, X. et al. Niche differentiation of comammox Nitrospira and canonical nitrifiers in riparian wetland ecosystems around Taihu Lake. J Soils Sediments 23, 2518–2528 (2023). https://doi.org/10.1007/s11368-023-03504-z

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