Applied Microbiology and Biotechnology

, Volume 101, Issue 21, pp 8015–8027 | Cite as

Multi-scale factors affecting composition, diversity, and abundance of sediment denitrifying microorganisms in Yangtze lakes

  • Xiaoliang Jiang
  • Lu Yao
  • Laodong Guo
  • Guihua Liu
  • Wenzhi Liu
Environmental biotechnology


Sediment denitrification is the dominant nitrogen removal pathway in many aquatic habitats and can be regulated by local-, landscape-, and regional-scale factors. However, the mechanisms for how these multiple scale factors and their interactions affect the sediment denitrifying communities remain poorly understood. In this study, we investigated the community composition, diversity, and abundance of nitrite reductase genes (nirK and nirS)-encoding denitrifiers in 74 sediment samples from 22 Yangtze lakes using clone library and quantitative PCR techniques. Information of location, climate, catchment land use, water quality, sediment properties, and plant communities at each sampling site was analyzed to elucidate the effects of regional, landscape, and local factors on the characteristics of sediment denitrifying communities. Results of canonical correspondence analysis indicated that local factors were the key determinants of denitrifying community composition, accounting for over 20% of the total variation. Additionally, certain regional and landscape factors, including elevation and catchment built-up land, were also significantly related to the composition of denitrifying communities. Variance partitioning analyses revealed that diversity and abundance in the nirK denitrifier community were largely influenced by local factors, while those in the nirS community were controlled by both local and regional factors. Our findings highlight the importance of using different scale factors to explain adequately the composition and structure of denitrifying communities in aquatic environments.


Denitrification Denitrifying community Land use Nitrogen cycles Yangtze River 



We thank Yujing Wu, Ziqian Xiong, and Bei Lu for their assistance with field work and sample processing.


This study was funded by the National Science Foundation of China (Grant number 31570535).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

253_2017_8537_MOESM1_ESM.pdf (280 kb)
ESM 1 (PDF 279 kb)


  1. Abell GCJ, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2010) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300CrossRefPubMedGoogle Scholar
  2. Attard E, Recous S, Chabbi A, De Berranger C, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Le Roux X (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Glob Chang Biol 17:1975–1989CrossRefGoogle Scholar
  3. Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775PubMedPubMedCentralGoogle Scholar
  4. Braker G, Matthies D, Hannig M, Brandt FB, Brenzinger K, Grongroft A (2015) Impact of land use management and soil properties on denitrifier communities of Namibian savannas. Microb Ecol 70:981–992CrossRefPubMedGoogle Scholar
  5. Bremer C, Braker G, Matthies D, Reuter A, Engels C, Conrad R (2007) Impact of plant functional group, plant species, and sampling time on the composition of nirK-type denitrifier communities in soil. Appl Environ Microbiol 73:6876–6884CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bru D, Ramette A, Saby NPA, Dequiedt S, Ranjard L, Jolivet C, Arrouays D, Philippot L (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5:532–542CrossRefPubMedGoogle Scholar
  7. Carpenter SR, Lodge DM (1986) Effects of submersed macrophytes on ecosystem processes. Aquat Bot 26:341–370CrossRefGoogle Scholar
  8. Chen Z, Luo X, Hu R, Wu M, Wu J, Wei W (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb Ecol 60:850–861CrossRefPubMedGoogle Scholar
  9. Clough Y, Kruess A, Kleijn D, Tscharntke T (2005) Spider diversity in cereal fields: comparing factors at local, landscape and regional scales. J Biogeogr 32:2007–2014CrossRefGoogle Scholar
  10. Dandie CE, Wertz S, Leclair CL, Goyer C, Burton DL, Patten CL, Zebarth BJ, Trevors JT (2011) Abundance, diversity and functional gene expression of denitrifier communities in adjacent riparian and agricultural zones. FEMS Microbiol Ecol 77:69–82CrossRefPubMedGoogle Scholar
  11. Dang H, Wang C, Li J, Li T, Tian F, Jin W, Ding Y, Zhang Z (2009) Diversity and distribution of sediment nirS-encoding bacterial assemblages in response to environmental gradients in the eutrophied Jiaozhou Bay, China. Microb Ecol 58:161–169CrossRefPubMedGoogle Scholar
  12. Dodson SI, Lillie RA, Will-Wolf S (2005) Land use, water chemistry, aquatic vegetation, and zooplankton community structure of shallow lakes. Ecol Appl 15:1191–1198CrossRefGoogle Scholar
  13. Enwall K, Throbäck IN, Stenberg M, Söderström M, Hallin S (2010) Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76:2243–2250CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fang J, Wang Z, Zhao S, Li Y, Tang Z, Yu D, Ni L, Liu H, Xie P, Da L (2006) Biodiversity changes in the lakes of the Central Yangtze. Front Ecol Environ 4:369–377CrossRefGoogle Scholar
  15. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631CrossRefPubMedPubMedCentralGoogle Scholar
  16. Francis CA, O'Mullan GD, Cornwell JC, Cornwell JC, Ward BB (2013) Transitions in nirS-type denitrifier diversity, community composition, and biogeochemical activity along the Chesapeake Bay estuary. Front Microbiol 4:37CrossRefGoogle Scholar
  17. Guo G, Deng H, Qiao M, Yao H, Zhu Y (2013) Effect of long-term wastewater irrigation on potential denitrification and denitrifying communities in soils at the watershed scale. Environ Sci Technol 47:3105–3113PubMedGoogle Scholar
  18. Guo L, Hu Z, Fang F, Liu T, Chuai X, Yang L (2014) Trophic status determines the nirS-denitrifier community in shallow freshwater lakes. Ann Microbiol 64:999–1006CrossRefGoogle Scholar
  19. Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 65:1652–1657PubMedPubMedCentralGoogle Scholar
  20. Harrison JA, Maranger RJ, Alexander RB, Giblin AE, Jacinthe PA, Mayorga E, Seitzinger SP, Sobota DJ, Wollheim WM (2009) The regional and global significance of nitrogen removal in lakes and reservoirs. Biogeochemistry 93:143–157CrossRefGoogle Scholar
  21. Herrmann M, Saunders AM, Schramm A (2009) Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Appl Environ Microbiol 75:3127–3136CrossRefPubMedPubMedCentralGoogle Scholar
  22. Heylen K, Gevers D, Vanparys B, Wittebolle L, Geets J, Boon N, De Vos P (2006) The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ Microbiol 8:2012–2021CrossRefPubMedGoogle Scholar
  23. Hou J, Cao X, Song C, Zhou Y (2013) Predominance of ammonia-oxidizing archaea and nirK-gene-bearing denitrifiers among ammonia-oxidizing and denitrifying populations in sediments of a large urban eutrophic lake (Lake Donghu). Can J Microbiol 59:456–464CrossRefPubMedGoogle Scholar
  24. Huang S, Chen C, Yang X, Wu Q, Zhang R (2011) Distribution of typical denitrifying functional genes and diversity of the nirS-encoding bacterial community related to environmental characteristics of river sediments. Biogeosciences 8:3041–3051CrossRefGoogle Scholar
  25. Kim OS, Imhoff JF, Witzel KP, Junier P (2011) Distribution of denitrifying bacterial communities in the stratified water column and sediment-water interface in two freshwater lakes and the Baltic Sea. Aquat Ecol 45:99–112CrossRefGoogle Scholar
  26. Knapp CW, Dodds WK, Wilson KC, O'Brien JM, Graham DW (2009) Spatial heterogeneity of denitrification genes in a highly homogenous urban stream. Environ Sci Technol 43:4273–4279CrossRefPubMedGoogle Scholar
  27. Li M, Hong Y, Cao H, Klotz MG, Gu JD (2013) Diversity, abundance, and distribution of NO-forming nitrite reductase-encoding genes in deep-sea subsurface sediments of the South China Sea. Geobiology 11:170–179CrossRefPubMedGoogle Scholar
  28. Ligi T, Truu M, Truu J, Nolvak H, Kaasik A, Mitsch WJ, Mander U (2014) Effects of soil chemical characteristics and water regime on denitrification genes (nirS, nirK, and nosZ) abundances in a created riverine wetland complex. Ecol Eng 72:47–55CrossRefGoogle Scholar
  29. Lindstrom ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4:1–9CrossRefPubMedGoogle Scholar
  30. Lindstrom ES, Forslund M, Algesten G, Bergstrom AK (2006) External control of bacterial community structure in lakes. Limnol Oceanogr 51:339–342CrossRefGoogle Scholar
  31. Liu W, Zhang Q, Liu G (2011) Effects of watershed land use and lake morphometry on the trophic state of Chinese lakes: implications for eutrophication control. Clean-Soil Air Water 39:35–42CrossRefGoogle Scholar
  32. Liu W, Li S, Bu H, Zhang Q, Liu G (2012) Eutrophication in the Yunnan Plateau lakes: the influence of lake morphology, watershed land use, and socioeconomic factors. Environ Sci Pollut Res 19:858–870CrossRefGoogle Scholar
  33. Liu W, Yao L, Wang Z, Xiong Z, Liu G (2015) Human land uses enhance sediment denitrification and N2O production in Yangtze lakes primarily by influencing lake water quality. Biogeosciences 12:6059–6070CrossRefGoogle Scholar
  34. Liu Y, Priscu JC, Xiong J, Conrad R, Vick-Majors T, Chu H, Hou J (2016) Salinity drives archaeal distribution patterns in high altitude lake sediments on the Tibetan Plateau. FEMS Microbiol Ecol 92:fiw033CrossRefPubMedGoogle Scholar
  35. Mao G, Chen L, Yang Y, Wu Z, Tong T, Liu Y, Xie S (2017) Vertical profiles of water and sediment denitrifiers in two plateau freshwater lakes. Appl Microbiol Biotechnol 101:3361–3370CrossRefPubMedGoogle Scholar
  36. Morrissey EM, Franklin RB (2015) Resource effects on denitrification are mediated by community composition in tidal freshwater wetlands soils. Environ Microbiol 17:1520–1532CrossRefPubMedGoogle Scholar
  37. Mosier AC, Francis CA (2010) Denitrifier abundance and activity across the San Francisco Bay estuary. Environ Microbiol Rep 2:667–676CrossRefPubMedGoogle Scholar
  38. Penton CR, Louis DS, Pham A, Cole JR, Wu L, Luo Y, Schuur EAG, Zhou J, Tiedje JM (2015) Denitrifying and diazotrophic community responses to artificial warming in permafrost and tallgrass prairie soils. Front Microbiol 6:746CrossRefPubMedPubMedCentralGoogle Scholar
  39. Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619CrossRefPubMedPubMedCentralGoogle Scholar
  40. Saarenheimo J, Tiirola MA, Rissanen AJ (2015) Functional gene pyrosequencing reveals core proteobacterial denitrifiers in boreal lakes. Front Microbiol 6:674CrossRefPubMedPubMedCentralGoogle Scholar
  41. Seitzinger S, Harrison JA, Bohlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090CrossRefPubMedGoogle Scholar
  42. Sirivedhin T, Gray KA (2006) Factors affecting denitrification rates in experimental wetlands: field and laboratory studies. Ecol Eng 26:167–181CrossRefGoogle Scholar
  43. Tatariw C, Chapman EL, Sponseller RA, Mortazavi B, Edmonds JW (2013) Denitrification in a large river: consideration of geomorphic controls on microbial activity and community structure. Ecology 94:2249–2262CrossRefPubMedGoogle Scholar
  44. Telford RJ, Vandvik V, Birks HJB (2006) Dispersal limitations matter for microbial morphospecies. Sci 312:1015–1015CrossRefGoogle Scholar
  45. Wang HT, Su JQ, Zheng TL, Yang X (2014) Impacts of vegetation, tidal process, and depth on the activities, abundances, and community compositions of denitrifiers in mangrove sediment. Appl Microbiol Biotechnol 98:9375–9387CrossRefPubMedGoogle Scholar
  46. Warneke S, Schipper LA, Matiasek MG, Scow KM, Cameron S, Bruesewitz DA, McDonald IR (2011) Nitrate removal, communities of denitrifiers and adverse effects in different carbon substrates for use in denitrification beds. Water Res 45:5463–5475CrossRefPubMedPubMedCentralGoogle Scholar
  47. Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, Yang Y, Yao T, Knight R, Chu H (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466CrossRefPubMedPubMedCentralGoogle Scholar
  48. Xiong Z, Li S, Yao L, Liu G, Zhang Q, Liu W (2015) Topography and land use effects on spatial variability of soil denitrification and related soil properties in riparian wetlands. Ecol Eng 83:437–443CrossRefGoogle Scholar
  49. Yang G, Ma R, Zhang L, Jiang J, Yao S, Zhang M, Zeng H (2010) Lake status, major problems and protection strategy in China. Scientia Limnologica Sinica 22:799–810 (in Chinese with English abstract)Google Scholar
  50. Yang J, Jiang H, Wu G, Liu W, Zhang G (2016) Distinct factors shape aquatic and sedimentary microbial community structures in the lakes of western China. Front Microbiol 7:1782PubMedPubMedCentralGoogle Scholar
  51. Yao H, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environ Microbiol 15:2545–2556CrossRefPubMedGoogle Scholar
  52. Yi N, Gao Y, Zhang Z, Shao H, Yan S (2015) Water properties influencing the abundance and diversity of denitrifiers on Eichhornia crassipes roots: a comparative study from different diffluent around Dianchi Lake, China. Int J Genom 2015:142197Google Scholar
  53. Zhang Y, Xie X, Jiao N, Hsiao SSY, Kao S (2014) Diversity and distribution of amoA-type nitrifying and nirS-type denitrifying microbial communities in the Yangtze River estuary. Biogeosciences 11:2131–2145CrossRefGoogle Scholar
  54. Zhao D, Luo J, Zeng J, Wang M, Yan W, Huang R, Wu Q (2014) Effects of submerged macrophytes on the abundance and community composition of ammonia-oxidizing prokaryotes in a eutrophic lake. Environ Sci Pollut Res 21:389–398CrossRefGoogle Scholar
  55. Zheng Y, Hou L, Liu M, Gao J, Yin G, Li X, Deng F, Lin X, Jiang X, Chen F (2015) Diversity, abundance, and distribution of nirS-harboring denitrifiers in intertidal sediments of the Yangtze Estuary. Microb Ecol 70:30–40CrossRefPubMedGoogle Scholar
  56. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Xiaoliang Jiang
    • 1
  • Lu Yao
    • 1
  • Laodong Guo
    • 2
  • Guihua Liu
    • 1
  • Wenzhi Liu
    • 1
    • 2
  1. 1.Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  2. 2.School of Freshwater SciencesUniversity of Wisconsin-MilwaukeeMilwaukeeUSA

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