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pH regulates ammonia-oxidizing bacteria and archaea in paddy soils in Southern China

  • Environmental biotechnology
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Abstract

Ammonia-oxidizing archaea (AOA) and bacteria (AOB) play important roles in nitrogen cycling. However, the effects of environmental factors on the activity, abundance, and diversity of AOA and AOB and the relative contributions of these two groups to nitrification in paddy soils are not well explained. In this study, potential nitrification activity (PNA), abundance, and diversity of amoA genes from 12 paddy soils in Southern China were determined by potential nitrification assay, quantitative PCR, and cloning. The results showed that PNA was highly variable between paddy soils, ranging from 4.05 ± 0.21 to 9.81 ± 1.09 mg NOx-N kg−1 dry soil day−1, and no significant correlation with soil parameters was found. The abundance of AOA was predominant over AOB, indicating that AOA may be the major members in aerobic ammonia oxidation in these paddy soils. Community compositions of AOA and AOB were highly variable among samples, but the variations were best explained by pH. AOA sequences were affiliated to the Nitrosopumilus cluster and Nitrososphaera cluster, and AOB were classified into the lineages of Nitrosospira and Nitrosomonas, with Nitrosospira being predominant over Nitrosomonas, accounting for 83.6 % of the AOB community. Moreover, the majority of Nitrosomonas was determined in neutral soils. Canonical correspondence analysis (CCA) analysis further demonstrated that AOA and AOB community structures were significantly affected by pH, soil total organic carbon, total nitrogen, and C/N ratio, suggesting that these factors exert strong effects on the distribution of AOB and AOA in paddy soils in Southern China. In conclusion, our results imply that soil pH was a key explanatory variable for both AOA and AOB community structure and nitrification activity.

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References

  • Alves RJE, Wanek W, Zappe A, Richter A, Svenning MM, Schleper C, Urich T (2013) Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea. ISME J 7:1620–1631. doi:10.1038/ismej.2013.35

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Avrahami S, Conrad R, Braker G (2002) Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers. Appl Environ Microbiol 68(11):5685–5692. doi:10.1128/AEM. 68.11.5685-5692.2002

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Boyle-Yarwood SA, Bottomley PJ, Myrold DD (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10(11):2956–2965. doi:10.1111/j.1462-2920.2008.01600.x

    Article  CAS  PubMed  Google Scholar 

  • Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1(7):660–662. doi:10.1038/ismej.2007.79

    Article  PubMed  Google Scholar 

  • Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10(8):1978–1987. doi:10.1111/j.1462-2920.2008.01613.x

    Article  CAS  PubMed  Google Scholar 

  • Chen XP, Zhang LM, Shen JP, Xu ZH, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10(8):1510–1516. doi:10.1007/s11368-010-0256-9

    Article  CAS  Google Scholar 

  • Chen XP, Zhang LM, Shen JP, Wei WX, He JZ (2011) Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil. Biol Fert Soils 47(3):323–331. doi:10.1007/s00374-011-0542-8

    Article  CAS  Google Scholar 

  • DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89(12):5685–5689. doi:10.1073/pnas.89.12.5685

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Di HJ, Cameron K, Shen JP, Winefield C, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2(9):621–624. doi:10.1038/ngeo613

    Article  CAS  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 U S A 102(41):14683–14688. doi:10.1073/pnas.0506625102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74(3):566–574. doi:10.1111/j.1574-6941.2010.00971.x

    Article  CAS  PubMed  Google Scholar 

  • Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3(5):597–605. doi:10.1038/ismej.2008.128

    Article  CAS  PubMed  Google Scholar 

  • Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008) A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U S A 105(6):2134–2139. doi:10.1073/pnas.0708857105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9(9):2364–2374. doi:10.1111/j.1462-2920.2007.01358.x

    Article  CAS  PubMed  Google Scholar 

  • Head IM, Hiorns WD, Embley TM, McCarthy AJ, Saunders JR (1993) The phylogeny of autotrophic ammonia-oxidizing bacteria as determined by analysis of 16S ribosomal RNA gene sequences. J Gen Microbiol 139(6):1147–1153. doi:10.1099/00221287-139-6-1147

    Article  CAS  PubMed  Google Scholar 

  • Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealedby high-throughput pyrosequencing. J Soil Sediment 13:1439–1449. doi:10.1007/s11368-013-0726-y

    Article  Google Scholar 

  • Hu BL, Liu S, Wang W, Shen LD, Lou LP, Liu WP, Tian GM, Xu XY, Zheng P (2014) pH-dominated niche segregation of ammonia-oxidising microorganisms in Chinese agricultural soils. FEMS Microbiol Ecol 90:290–299. doi:10.1111/1574-6941.12391

    Article  CAS  Google Scholar 

  • Huang R, Wu Y, Zhang J, Zhong W, Jia Z, Cai Z (2012) Nitrification activity and putative ammonia-oxidizing archaea in acidic red soils. J Soil Sediment 12(3):420–428. doi:10.1007/s11368-011-0450-4

    Article  CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than archaea dominate microbial ammoniaoxidation in an agricultural soil. Environ Microbiol 11(7):1658–1671. doi:10.1111/j.1462-2920.2009.01891.x

  • Jiang XJ, Hou XY, Zhou X, Xin XP, Wright A, Jia ZJ (2015) pH regulates key players of nitrification in paddy soils. Soil Biol Biochem 81:9–16. doi:10.1016/j.soilbio.2014.10.025

    Article  CAS  Google Scholar 

  • Jin T, Zhang T, Ye L, Lee OO, Wong YH, Qian PY (2011) Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River Estuary, China. Appl Microbiol Biotechnol 90(3):1137–1145. doi:10.1007/s00253-011-3107-8

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G, Prosser J, Schuster S, Schleper C (2006) Archaea predominate amongammonia-oxidizing prokaryotes in soils. Nature 442:806–809. doi:10.1038/nature04983

    Article  CAS  PubMed  Google Scholar 

  • Li M, Cao H, Hong Y, Gu JD (2011) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89(4):1243–1254. doi:10.1007/s00253-010-2929-0

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y-C, Liu B-R, Li S-H, Qin H, Fu W-J, Xu Q-F (2014) Shift in abundance and structure of soil ammonia-oxidizing bacteria and archaea communities associated with four typical forest vegetations in subtropical region. J Soil Sediment 14:1577-1586. doi:10.1007/s11368-014-0902-8

  • Long XE, Chen C, Xu Z, He JZ (2014) Shifts in the abundance and community structure of soil ammonia oxidizers in a wet sclerophyll forest under long-term prescribed burning. Sci Total Environ 470:578–586. doi:10.1016/j.scitotenv.2013.10.011

    Article  PubMed  Google Scholar 

  • Molina V, Belmar L, Ulloa O (2010) High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygen-deficient waters of the eastern South Pacific. Environ Microbiol 12(9):2450–2465. doi:10.1111/j.1462-2920.2010.02218.x

    Article  CAS  PubMed  Google Scholar 

  • Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10(11):3002–3016. doi:10.1111/j.1462-2920.2008.01764.x

    Article  CAS  PubMed  Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microb 59(3):695–700

    CAS  Google Scholar 

  • Nakagawa T, Mori K, Kato C, Takahashi R, Tokuyama T (2007) Distribution of cold-adapted ammonia-oxidizing microorganisms in the deep-ocean of the northeastern Japan Sea. Microbes Environ 22:365–372. doi:10.1264/jsme2.22.365

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environl Microbiol 10(11):2966–2978. doi:10.1111/j.1462-2920.2008.01701.x

    Article  CAS  Google Scholar 

  • Nicolaisen MH, Risgaard-Petersen N, Revsbech NP, Reichardt W, Ramsing NB (2004) Nitrification-denitrification dynamics and community structure of ammonia oxidizing bacteria in a high yield irrigated Philippine rice field. FEMS Microbiol Ecol 49(3):359–369. doi:10.1016/j.femsec.2004.04.015

    Article  CAS  PubMed  Google Scholar 

  • Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B, Lebauer D, Scow KM (2004) Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microb 70(2):1008–1016. doi:10.1128/AEM. 70.2.1008-1016.2004

    Article  CAS  Google Scholar 

  • Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14(2):525–539. doi:10.1111/j.1462-2920.2011.02666.x

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20(11):523–531. doi:10.1016/j.tim.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  • Purkhold U, Wagner M, Timmermann G, Pommerening-Röser A, Koops H-P (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the Nitrosomonads. Int J Syst Evol Micr 53(5):1485–1494. doi:10.1099/ijs. 0.02638-0

  • 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 Microb 63(12):4704–4712

    CAS  Google Scholar 

  • Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizingbacteria and archaea across physicochemical gradients in asubterranean estuary. Environ Microbioll 10:1068–1079. doi:10.1111/j.1462-2920.2007.01547.x

    Article  CAS  Google Scholar 

  • Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488. doi:10.1038/nrmicro1159

    Article  CAS  PubMed  Google Scholar 

  • Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10(6):1601–1611. doi:10.1111/j.1462-2920.2008.01578.x

    Article  CAS  PubMed  Google Scholar 

  • Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3(296):1–7. doi:10.3389/fmicb.2012.00296

    Google Scholar 

  • Shen C, Xiong J, Zhang H, Feng Y, Lin X, Li X, Liang W, Chu H (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211. doi:10.1016/j.soilbio.2012.07.013

    Article  CAS  Google Scholar 

  • Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5(6):1067–1071. doi:10.1038/ismej.2010.191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang Y, Ke X, Wu L, Lu Y (2009) Community composition of ammonia-oxidizing bacteria and archaea in rice field soil as affected by nitrogen fertilization. Syst Appl Microbiol 32(1):27–36. doi:10.1016/j.syapm.2008.09.007

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wang Y, Feng X, Zhai L, Zhu G (2011) Quantitative analyses of ammonia-oxidizing archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Appl Microbiol Biotechnol 90(2):779–787. doi:10.1007/s00253-011-3090-0

  • Wang J, Wang W, Gu JD (2014) Community structure and abundance of ammonia-oxidizing archaea and bacteria after conversion from soybean to rice paddy in albic soils of Northeast China. Appl Microbiol Biotechnol 98:2765–2778. doi:10.1007/s00253-013-5213-2

    Article  CAS  PubMed  Google Scholar 

  • Wang HT, Su JQ, Zheng TL, Yang XR (2015) Insights into the role of plant on ammonia-oxidizing bacteriaand archaea in the mangrove ecosystem. J Soil Sediment. doi:10.1007/s11368-015-1074-x

    Google Scholar 

  • Ward BB, O'Mullan GD (2002) Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing γ-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl Environ Microbiol 68(8):4153–4157. doi:10.1128/AEM. 68.8.4153-4157.2002

  • Wessén E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45(3):193–200. doi:10.1016/j.apsoil.2010.04.003

    Article  Google Scholar 

  • Wu Y, Lu L, Wang B, Lin X, Zhu J, Cai Z, Yan X, Jia Z (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75(4):1431–1439. doi:10.2136/sssaj2010.0434

    Article  CAS  Google Scholar 

  • Yang XR, Li H, Nie SA, Su JQ, Weng BS, Zhu GB, Yao HY, Gilbert JA, Zhu YG (2015) Potential contribution of anammox to nitrogen loss from paddy soils in Southern China. Appl Environ Microb 81(3):938–947. doi:10.1128/AEM. 02664-14

    Article  CAS  Google Scholar 

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microb 77(13):4618–4625. doi:10.1128/AEM. 00136-11

    Article  CAS  Google Scholar 

  • Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6(5):1032–1045. doi:10.1038/ismej.2011.168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Natural Science Foundation of China (41090282, 41401297, 31270153), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB15020302, XDB15020402), the China Postdoctoral Science Foundation (2014 M551846), and the International Science and Technology Cooperation Program of China (2011DFB91710).

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  1. Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen, 361021, China

    Hu Li, Bo-Sen Weng, Fu-Yi Huang, Jian-Qiang Su & Xiao-Ru Yang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Hu Li

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  1. Hu Li
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Li, H., Weng, BS., Huang, FY. et al. pH regulates ammonia-oxidizing bacteria and archaea in paddy soils in Southern China. Appl Microbiol Biotechnol 99, 6113–6123 (2015). https://doi.org/10.1007/s00253-015-6488-2

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