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Determinants of the biodiversity patterns of ammonia-oxidizing archaea community in two contrasting forest stands

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The variation in soil microbial community patterns is primarily influenced by ecological processes associated with spatial distance and environmental heterogeneities. However, the relative importance of these processes in determining the patterns of soil microbial biodiversity in different successional forests remains unclear.

Materials and methods

Based on the species data from denaturing gradient gel electrophoresis (DGGE) analysis, we described the composition and beta diversity of ammonia-oxidizing archaea (AOA) community, an important functional microbial group in regulating nitrogen cycle, in a middle-succeed stand (60 years of secondary succession) and an undisturbed native stand in a subtropical forest in southern China. The composition pattern was examined using a multi-response permutation procedure (MRPP), and the beta diversity was described using the Sørensen index. The relative influence of edaphic, vegetational, spatial, and topographical factors on AOA composition and beta diversity was assessed by variation partitioning and multiple regression on distance matrices (MRM), respectively.

Results and discussion

We did not find any stand-specific patterns in AOA community composition in the two stands; however, the influential variables were different between the two stands; 7.3 and 4.5 % of the total variation in AOA community composition could be explained by edaphic (i.e., available potassium and total phosphorus) and spatial variables, respectively, in the middle-succeed stand, while 3.7 and 2.8 % of the variation were explained by spatial variable and available phosphorus, respectively, in the native stand. Soil total phosphorus influenced the beta diversity of AOA community most in the middle-succeed stand, while genetic distance of tree species was found to be the most important factor in driving the beta diversity pattern in the native stand.


Soil nutrients influenced the beta diversity of AOA community in the middle-succeed stand more than that in the native stand, while vegetation is more important in the native stand. The substantial unexplained variations were possibly due to the effects of other unmeasured variables. Nevertheless, dispersal process is more important in controlling AOA community composition in the native stand, while processes associated with environmental heterogeneities are more important in the middle-succeed stand in this subtropical forest.

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  1. Bahram M, Koljalg U, Courty PE et al (2013) The distance decay of similarity in communities of ectomycorrhizal fungi in different ecosystems and scales. J Ecol 101:1335–1344

  2. Borcard D, Legendre P (1994) Environmental control and spatial structure in ecological communities: an example using oribatid mites (Acari, Oribatei). Environ Ecol Stat 1:37–61

  3. Brant JB, Myrold DD, Sulzman EW (2006) Root controls on soil microbial community structure in forest soils. Oecologia 148:650–659

  4. Bru D, Ramette A, Saby NPA et al (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5:532–542

  5. Chen XF, Li ZP, Liu M et al (2015) Microbial community and functional diversity associated with different aggregate fractions of a paddy soil fertilized with organic manure and/or NPK fertilizer for 20 years. J Soil Sediment 15:292–301

  6. Dang H, Li J, Zhang X et al (2009) Diversity and spatial distribution ofamoA-encoding archaea in the deep-sea sediments of the tropical West Pacific Continental Margin. J Appl Microbiol 106:1482–1493

  7. de Gannes V, Eudoxie G, Hickey WJ (2014) Impacts of edaphic factors on communities of ammonia-oxidizing archaea, ammonia-oxidizing bacteria and nitrification in tropical soils. PLoS One 9(2):e89568

  8. Di HJ, Cameron KC, Shen JP et al (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394

  9. Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196:483–493

  10. Dumbrell AJ, Nelson M, Helgason T et al (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:1078–1078

  11. Fang YT, Yoh M, Koba K et al (2011) Nitrogen deposition and forest nitrogen cycling along an urban–rural transect in southern China. Glob Change Biol 17:872–885

  12. Flinn KM, Lechowicz MJ, Waterway MJ (2008) Plant species diversity and composition of wetlands within an upland forest. Am J Bot 95:1216–1224

  13. Florencio M, Diaz-Paniagua C, Gomez-Rodriguez C, Serrano L (2014) Biodiversity patterns in a macroinvertebrate community of a temporary pond network. Insect Conserv Diver 7:4–21

  14. Fu QL, Liu C, Ding NF et al (2012) Soil microbial communities and enzyme activities in a reclaimed coastal soil chronosequence under rice-barley cropping. J Soil Sediment 12:1134–1144

  15. Gilbert B, Bennett JR (2010) Partitioning variation in ecological communities: do the numbers add up? J Appl Ecol 47:1071–1082

  16. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

  17. Haichar FE, Marol C, Berge O et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

  18. Hatzenpichler R (2012) Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microb 78:7501–7510

  19. Hedin LO, Vitousek PM, Matson PA (2003) Nutrient losses over four million years of tropical forest development. Ecology 84:2231–2255

  20. Hooper DU, Bignell DE, Brown VK et al (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 50:1049–1061

  21. Hu CJ, Fu BJ, Liu GH et al (2010) Vegetation patterns influence on soil microbial biomass and functional diversity in a hilly area of the Loess Plateau, China. J Soil Sediment 10:1082–1091

  22. Huang WJ, Liu JX, Tang XL et al (2009) Inorganic nitrogen and available phosphorus concentrations in the soils of five forests at Dinghushan, China*. Chinese J of Appplied Environ Biol 2009:441–447 (in Chinese)

  23. Isobe K, Koba K, Suwa Y et al (2012) High abundance of ammonia-oxidizing archaea in acidified subtropical forest soils in southern China after long-term N deposition. Fems Microbiol Ecol 80:193–203

  24. Keiser AD, Strickland MS, Fierer N, Bradford MA (2011) The effect of resource history on the functioning of soil microbial communities is maintained across time. Biogeosciences 8:1477–1486

  25. Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence-absence data. J Anim Ecol 72:367–382

  26. Konneke M, Bernhard AE, de la Torre JR et al (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

  27. Krsek M, Wellington EMH (1999) Comparison of different methods for the isolation and purification of total community DNA from soil. J Microbiol Meth 39:1–16

  28. Legendre P, Lapointe FJ, Casgrain P (1994) Modelling brain evolution from behavior: a permutational regression approach. Evolution 48:1487–1499

  29. Li JJ, Zheng YM, Yan JX et al (2013) Succession of plant and soil microbial communities with restoration of abandoned land in the Loess Plateau, China. J Soil Sediment 13:760–769

  30. Liang Y, He X, Liang S et al (2014) Community structure analysis of soil ammonia oxidizers during vegetation restoration in southwest China. J Basic Microb 54:180–189

  31. Lichstein JW (2007) Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecol 188:117–131

  32. Liu GS, Jiang NH, Zhang LD, Liu ZL (1996) Soil physical and chemical analysis and description of soil profiles. China Standards Press, Beijing

  33. Liu J, Yan HF, Newmaster SG et al (2015) The use of DNA barcoding as a tool for the conservation biogeography of subtropical forests in China. Divers Distrib 21:188–199

  34. Liu KH, Fang YT, Yu FM et al (2010) Soil acidification in response to acid deposition in three subtropical forests of subtropical China. Pedosphere 20:399–408

  35. Liu L, Zhang T, Gilliam FS et al (2013) Interactive effects of nitrogen and phosphorus on soil microbial communities in a tropical forest. PLoS One 8(4):e61188

  36. Liu WP, Cao HL, Liu W et al (2011) Study on diversity of monsoon evergreen broad leaved forest in different kinds of habitat in Dinghushan. J of Anhui Agri Sci 39:16159–16163 (in Chinese)

  37. Lu L, Jia Z (2013) Urease gene-containing Archaeadominate autotrophic ammonia oxidation in two acid soils. Environ Microbiol 15:1795–1809

  38. Ma L, Chen C, Shen Y et al (2014) Determinants of tree survival at local scale in a sub-tropical forest. Ecol Res 29:69–80

  39. Madritch MD, Hunter MD (2002) Phenotypic diversity influences ecosystem functioning in an oak sandhills community. Ecology 83:2084–2090

  40. Martiny JBH, Bohannan BJM, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

  41. Martiny JBH, Eisen JA, Penn K et al (2011) Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci U S A 108:7850–7854

  42. McArthur JV, Kovacic DA, Smith MH (1988) Genetic diversity in natural populations of a soil bacterium across a landscape gradient. Proc Natl Acad Sci U S A 85:9621–9624

  43. McCaig AE, Glover LA, Prosser JI (2001) Numerical analysis of grassland bacterial community structure under different land management regimens by using 16S ribosomal DNA sequence data and denaturing gradient gel electrophoresis banding patterns. Appl Environ Microb 67:4554–4559

  44. Merila P, Malmivaara-Lamsa M, Spetz P et al (2010) Soil organic matter quality as a link between microbial community structure and vegetation composition along a successional gradient in a boreal forest. Appl Soil Ecol 46:259–267

  45. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16s ribosomal-RNA. Appl Environ Microb 59:695–700

  46. 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. Environ Microbiol 10:2966–2978

  47. O’Hanlon R, Harrington TJ (2012) Macrofungal diversity and ecology in four Irish forest types. Fungal Ecol 5:499–508

  48. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625

  49. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

  50. Ramette A, Tiedje JM (2007) Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. Proc Natl Acad Sci U S A 104:2761–2766

  51. Saetre P (1999) Spatial patterns of ground vegetation, soil microbial biomass and activity in a mixed spruce-birch stand. Ecography 22:183–192

  52. Schweitzer JA, Bailey JK, Fischer DG et al (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781

  53. Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Oxford

  54. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

  55. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

  56. Treusch AH, Leininger S, Kletzin A et al (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

  57. Wang JJ, Wu YC, Jiang HC et al (2008) High beta diversity of bacteria in the shallow terrestrial subsurface. Environ Microbiol 10:2537–2549

  58. Wang JT, Zheng YM, Hu HW et al (2015) Soil pH determines the alpha diversity but not beta diversity of soil fungal community along altitude in a typical Tibetan forest ecosystem. J Soil Sediment 15:1224–1232

  59. Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

  60. Wessen E, Soderstrom M, Stenberg M et al (2011) Spatial distribution of ammonia-oxidizing bacteria and archaea across a 44-hectare farm related to ecosystem functioning. ISEM J 5:1213–1225

  61. Yan ER, Wang XH, Huang JJ et al (2007) Long-lasting legacy of forest succession and forest management: Characteristics of coarse woody debris in an evergreen broad-leaved forest of Eastern China. Forest Ecol Manag 252:98–107

  62. Zhalnina K, de Quadros PD, Camargo FA, Triplett EW (2012) Drivers of archaeal ammonia-oxidizing communities in soil. Front Microbiol 3:210

  63. 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. ISEM J 6:1032–1045

  64. Zhao Y, Zhou ZH, Li W et al (2005) DNA extraction from soil for molecular microbial community analysis. J of Agro-Environ sci 24:854–860 (in Chinese)

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We thank Lin-fang Wu, Lei Ma, Yong Shen, Lan-ying Wang, Bo Kong, and Pi Luo for their help in sample collection; Tao-tao Li for the help in molecular experiments; and Peng zhu, SP Davis, Jr and Brittany Benjamin for their help in improving the language quality and readability. This work was supported by the Natural Science Foundation of China (NSFC-31370437, 31290222).

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Correspondence to Wei Liu.

Additional information

Jie Chen and Yichao Rui contributed equally to this study.

Responsible editor: Weijin Wang

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Chen, J., Rui, Y., Zhou, X. et al. Determinants of the biodiversity patterns of ammonia-oxidizing archaea community in two contrasting forest stands. J Soils Sediments 16, 878–888 (2016).

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  • Ammonia-oxidizing archaea
  • Beta diversity
  • Forest succession
  • Genetic distance
  • MRM
  • Subtropical forests