Advertisement

The Science of Nature

, 104:43 | Cite as

Responses of soil N-fixing bacteria communities to invasive plant species under different types of simulated acid deposition

  • Congyan WangEmail author
  • Jiawei Zhou
  • Kun Jiang
  • Jun Liu
  • Daolin DuEmail author
Original Paper

Abstract

Biological invasions have incurred serious threats to native ecosystems in China, and soil N-fixing bacteria communities (SNB) may play a vital role in the successful plant invasion. Meanwhile, anthropogenic acid deposition is increasing in China, which may modify or upgrade the effects that invasive plant species can cause on SNB. We analyzed the structure and diversity of SNB by means of new generation sequencing technology in soils with different simulated acid deposition (SAD), i.e., different SO4 2− to NO3 ratios, and where the invasive (Amaranthus retroflexus L.) and the native species (Amaranthus tricolor L.) grew mixed or isolated for 3 months. A. retroflexus itself did not exert significant effects on the diversity and richness of SNB but did it under certain SO4 2− to NO3 ratios. Compared to soils where the native species grew isolated, the soils where the invasive A. retroflexus grew isolated showed lower relative abundance of some SNB classes under certain SAD treatments. Some types of SAD can alter soil nutrient content which in turn could affect SNB diversity and abundance. Specifically, greater SO4 2− to NO3 ratios tended to have more toxic effects on SNB likely due to the higher exchange capacity of hydroxyl groups (OH) between SO4 2− and NO3 . As a conclusion, it can be expected a change in the structure of SNB after A. retroflexus invasion under acid deposition rich in sulfuric acid. This change may create a plant soil feedback favoring future A. retroflexus invasions.

Keywords

Amaranthus retroflexus L. Invasive plant species Simulated acid deposition Soil N-fixing bacteria communities 

Notes

Acknowledgements

We greatly appreciate to BioMarker Technologies Co., Ltd., Beijing, People’s Republic of China, for the determination of soil N-fixing bacteria community structure using high throughput sequencing. This study was supported by the National Natural Science Foundation of China (31300343, 31570414), Natural Science Foundation of Jiangsu Province, China (BK20130500), and Universities Natural Science Research Project of Jiangsu Province, China (13KJB610002). We are very grateful to the anonymous reviewer for the insightful and constructive comments that greatly improved this manuscript.

Supplementary material

114_2017_1463_MOESM1_ESM.doc (140 kb)
ESM 1 (DOC 140 kb)

References

  1. Bachelot B, Uriarte M, Zimmerman JK, Thompson J, Leff JW, Asiaii A, Koshner J, McGuire K (2016) Long-lasting effects of land use history on soil fungal communities in second-growth tropical rain forests. Ecol Appl 26:1881–1895. doi: 10.1890/15-1397.1 CrossRefPubMedGoogle Scholar
  2. Bagwell CE, Lovell CR (2000) Persistence of selected Spartina alterniflora rhizoplane diazotrophs exposed to natural and manipulated environmental variability. Appl Environ Microb 66:4625–4633. doi: 10.1128/AEM.66.11.4625-4633.2000 CrossRefGoogle Scholar
  3. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. doi: 10.1038/nmeth.2276 CrossRefPubMedGoogle Scholar
  4. Callaway RM, Bedmar EJ, Reinhart KO, Silvan CG, Klironomos J (2011) Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens. Ecology 92:1027–1035. doi: 10.1890/10-0089.1 CrossRefPubMedGoogle Scholar
  5. Carey CJ, Beman JM, Eviner VT, Malmstrom CM, Hart SC (2015) Soil microbial community structure is unaltered by plant invasion, vegetation clipping, and nitrogen fertilization in experimental semi-arid grasslands. Front Microbiol 6:466. doi: 10.3389/fmicb.2015.00466 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Castro-Díez P, Godoy O, Alonso A, Gallardo A, Saldaña A (2014) What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol Lett 17:1–12. doi: 10.1111/ele.12197 CrossRefPubMedGoogle Scholar
  7. Chao A, Chazdon RL, Colwell RK, Shen T-J (2005) A new statistical approach for assessing compositional similarity based on incidence and abundance data. Ecol Lett 8:148–159. doi: 10.1111/j.1461-0248.2004.00707.x CrossRefGoogle Scholar
  8. Chen J, Wang WH, Liu TW, Wu FH, Zheng HL (2013) Photosynthetic and antioxidant responses of Liquidambar formosana and Schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain. Plant Physiol Bioch 64:41–51. doi: 10.1016/j.plaphy.2012.12.012 CrossRefGoogle Scholar
  9. Chen T, Liu WL, Zhang CB, Wang J (2012) Effects of Solidago canadensis invadation on dynamics of native plant communities and their mechanisms. Chin J Plant Ecol 36:253–261. doi: 10.3724/SP.J.1258.2012.00253 CrossRefGoogle Scholar
  10. Christ M, Zhang YM, Likens GE, Driscoll CT (1995) Nitrogen retention capacity of a northern hardwood forest soil under ammonium sulfate additions. Ecol Appl 5:802–812. doi: 10.2307/1941988 CrossRefGoogle Scholar
  11. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The ribosomal database project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:D294–D296. doi: 10.1093/nar/gki038 CrossRefPubMedGoogle Scholar
  12. Costea M, Weaver SE, Tardif FJ (2004) The biology of Canadian weeds. 130. Amaranthus retroflexus L., A. powellii S. Watson and A. hybridus L.. Can J Plant Sci 84:631–668. doi: 10.4141/P02-183 CrossRefGoogle Scholar
  13. Dassonville N, Guillaumaud N, Piola F, Meerts P, Poly F (2011) Niche construction by the invasive Asian knotweeds (species complex Fallopia): impact on activity, abundance and community structure of denitrifiers and nitrifiers. Biol Invasions 13:1115–1133. doi: 10.1007/s10530-011-9954-5 CrossRefGoogle Scholar
  14. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431. doi: 10.1111/j.1461-0248.2011.01596.x CrossRefPubMedGoogle Scholar
  15. Duprè C, Stevens CJ, Ranke T, Bleeker A, Peppler-Lisbach C, Gowing DJG, Dise NB, Dorland E, Bobbink R, Diekmann M (2010) Changes in species richness and composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Glob Chang Biol 16:344–357. doi: 10.1111/j.1365-2486.2009.01982.x CrossRefGoogle Scholar
  16. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi: 10.1093/bioinformatics/btr38 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523. doi: 10.1007/s10021-002-0151-3 CrossRefGoogle Scholar
  18. Fan L, Chen Y, Yuan JG, Yang ZY (2010) The effect of Lantana camara Linn. invasion on soil chemical and microbiological properties and plant biomass accumulation in southern China. Geoderma 154:370–378. doi: 10.1016/j.geoderma.2009.11.010 CrossRefGoogle Scholar
  19. Hang ZH, Wu HP (2016) Zhenjiang Yearbook (The first edition). Organized by Zhenjiang Municipal People’s Government & Writed by Zhenjiang Local Records Office (Vol. 25). In: Chen J, Liu S (eds). Publishing House of Local Records, Beijing, p 27Google Scholar
  20. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan JM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microb 67:4399–4406. doi: 10.1128/AEM.68.1.448 CrossRefGoogle Scholar
  21. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898. doi: 10.1111/j.1462-2920.2010.02193.x CrossRefPubMedPubMedCentralGoogle Scholar
  22. Inderjit, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519. doi: 10.1016/j.tree.2010.06.006
  23. Jiang MS, Shi DP, Chen Y (2011) An analysis of acid rain distribution characteristics of five cities in south Jiangsu in recent five years. J Meteor Sci 31:99–104 (In Chinese)Google Scholar
  24. Kuebbing SE, Classen AT, Simberloff D (2014) Two co-occurring invasive woody shrubs alter soil properties and promote subdominant invasive species. J Appl Ecol 51:124–133. doi: 10.1111/1365-2664.12161 CrossRefGoogle Scholar
  25. Lau JA, Suwa T (2016) The changing nature of plant–microbe interactions during a biological invasion. Biol Invasions 18:3527–3534. doi: 10.1007/s10530-016-1245-8 CrossRefGoogle Scholar
  26. Laungani R, Knops JMH (2009) Species-driven changes in nitrogen cycling can provide a mechanism for plant invasions. Proc Natl Acad Sci U S A 106:12400–12405. doi: 10.1111/1365-2664.12161 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lei NF, Li J, Ni SJ, Chen JS (2014) Effects of clonal integration on microbial community composition and processes in the rhizosphere of the stoloniferous herb Glechoma longituba (Nakai) Kuprian. PLoS One 9:e108259. doi: 10.1371/journal.pone.0108259 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lindsay EA, Colloff MJ, Gibb NL, Wakelin SA (2010) The abundance of microbial functional genes in grassy woodlands is influenced more by soil nutrient enrichment than by recent weed invasion or livestock exclusion. Appl Environ Microb 76:5547–5555. doi: 10.1128/AEM.03054-09 CrossRefGoogle Scholar
  29. Liu ZQ, Chen JL (2007) Research on present situation and development tendency of atmospheric environmental quality in China. Electric Power Environ Prot 23:23–27 (In Chinese)Google Scholar
  30. Lv YN, Wang CY, Jia YY, Wang WW, Ma X, Du JJ, Pu GZ, Tian XJ (2014) Effects of sulfuric, nitric, and mixed acid rain on litter decomposition, soil microbial biomass, and enzyme activities in subtropical forests in China. Appl Soil Ecol 79:1–9. doi: 10.1016/j.apsoil.2013.12.002 CrossRefGoogle Scholar
  31. Ma JH, Xing GF, Yang WX, Ma LL, Gao M, Wang YG, Han YH (2012) Inhibitory effects of leachate from Eupatorium adenophorum on germination and growth of Amaranthus retroflexus and Chenopodium glaucum. Acta Ecol Sinica 32:50–56. doi: 10.1016/j.chnaes.2011.12.004 CrossRefGoogle Scholar
  32. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. doi: 10.1093/bioinformatics/btr50 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mandák B, Zákravský P, Dostál P, Plačková I (2011) Population genetic structure of the noxious weed Amaranthus retroflexus in Central Europe. Flora 206:697–703. doi: 10.1016/j.flora. 2011.01.010 CrossRefGoogle Scholar
  34. Mao YJ, Yannarell AC, Mackie RI (2011) Changes in N-transforming archaea and bacteria in soil during the establishment of bioenergy crops. PLoS One 6:e24750. doi: 10.1371/journal.pone.0024750 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Matzek V (2012) Trait values, not trait plasticity, best explain invasive species’ performance in a changing environment. PLoS One 7:e48821. doi: 10.1371/journal.pone.0048821 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mishra A, Singh AK, Singh KA, Pandey P, Yadav S, Khan AH, Barman SC (2012) Urban air pollution and their effects on rain water characteristics in Lucknow city, India. J Environ Res Deve 6:1127–1132Google Scholar
  37. Niro E, Marzaioli R, De Crescenzo S, D’Abrosca B, Castaldi S, Esposito A, Fiorentino A, Rutigliano FA (2016) Effects of the allelochemical coumarin on plants and soil microbial community. Soil Biol Biochem 95:30–39. doi: 10.1016/j.soilbio.2015.11.028 CrossRefGoogle Scholar
  38. Piper CL, Siciliano SD, Winsley T, Lamb EG (2015) Smooth brome invasion increases rare soil bacterial species prevalence, bacterial species richness and evenness. J Ecol 103:386–396. doi: 10.1111/1365-2745.12356 CrossRefGoogle Scholar
  39. Poly F, Ranjard L, Nazaret S, Gourbière F, Monrozier LJ (2001) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microb 67:2255–2262. doi: 10.1128/AEM.67.5.2255-2262.2001 CrossRefGoogle Scholar
  40. Riley D, Barber SA (1969) Bicarbonate accumulation and pH changes at the soybean (Glycine max (L.) Merr.) root-soil interface. Soil Sci Soc Am J 33:905–908CrossRefGoogle Scholar
  41. Riley D, Barber SA (1970) Salt accumulation at the soybean (Glycine max. (L.) Merr.) root-soil interface. Soil Sci Soc Am J 34:154–155CrossRefGoogle Scholar
  42. Rodrigues RR, Pineda RP, Barney JN, Nilsen ET, Barrett JE, Williams MA (2015) Plant invasions associated with change in root-zone microbial community structure and diversity. PLoS One 10:e141424. doi: 10.1371/journal.pone.0141424 Google Scholar
  43. Rodrigues VD, Torres TT, Ottoboni LMM (2014) Bacterial diversity assessment in soil of an active Brazilian copper mine using high-throughput sequencing of 16S rDNA amplicons. Anton Leeuwe 106:879–890. doi: 10.1007/s10482-014-0257-6 CrossRefGoogle Scholar
  44. Rodríguez-Echeverría S (2010) Rhizobial hitchhikers from down under: invasional meltdown in a plant-bacteria mutualism? J Biogeogr 37:1611–1622. doi: 10.1111/j.1365-2699.2010.02284.x Google Scholar
  45. Rodríguez-Echeverria S, Crisostomo JA, Nabais C, Freitas H (2009) Belowground mutualists and the invasive ability of Acacia longifolia in coastal dunes of Portugal. Biol Invasions 11:651–661. doi: 10.1007/s10530-008-9280-8 CrossRefGoogle Scholar
  46. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608. doi: 10.1038/ismej.2011.38 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sanon A, Beguiristain T, Cébron A, Berthelin J, Sylla SN, Duponnois R (2012) Differences in nutrient availability and mycorrhizal infectivity in soils invaded by an exotic plant negatively influence the development of indigenous Acacia species. J Environ Manag 95:S275–S279. doi: 10.1016/j.jenvman.2011.01.025 CrossRefGoogle Scholar
  48. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864. doi: 10.1093/bioinformatics/btr026 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Shen WS, Gao N, Min J, Shi WM, He XH, Lin XG (2016) Influences of past application rates of nitrogen and a catch crop on soil microbial communities between an intensive rotation. Acta Agr Scand B 66:97–106. doi: 10.1080/09064710.2015.1072234 Google Scholar
  50. Si CC, Liu XY, Wang CY, Wang L, Dai ZC, Qi SS, Du DL (2013) Different degrees of plant invasion significantly affect the richness of the soil fungal community. PLoS One 8:e85490. doi: 10.1371/journal.pone.0085490 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Simpson EH (1949) Measurement of diversity. Nature 163:688. doi: 10.1038/163688a0 CrossRefGoogle Scholar
  52. van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, Logtestijin R, Staehelin C (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178–187. doi: 10.1111/j.1574-6941.2006.00086.x CrossRefPubMedGoogle Scholar
  53. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Perg J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. doi: 10.1111/j.1461-0248.2011.01628.x CrossRefPubMedGoogle Scholar
  54. Wang CY, Guo P, Han GM, Feng XG, Zhang P, Tian XJ (2010) Effect of simulated acid rain on the litter decomposition of Quercus acutissima and Pinus massoniana in forest soil microcosms and the relationship with soil enzyme activities. Sci Total Environ 408:2706–2713. doi: 10.1016/j.scitotenv.2010.03.023 CrossRefPubMedGoogle Scholar
  55. Wang CY, Han GM, Jia Y, Feng XG, Guo P, Tian XJ (2011) Response of litter decomposition and related soil enzyme activities to different forms of nitrogen fertilization in a subtropical forest. Ecol Res 26:505–513. doi: 10.1007/s11284-011-0805-8 CrossRefGoogle Scholar
  56. Wang CY, Xiao HG, Liu J, Zhou JW, Du DL (2016b) Insights into the effects of simulated nitrogen deposition on leaf functional traits of Rhus typhina. Pol J Environ Stud 25:1279–1284. doi: 10.15244/pjoes/61788 CrossRefGoogle Scholar
  57. Wang CY, Xiao HG, Zhao LL, Liu J, Wang L, Zhang F, Shi YC, Du DL (2016a) The allelopathic effects of invasive plant Solidago canadensis on seed germination and growth of Lactuca sativa enhanced by different types of acid deposition. Ecotoxicology 25:555–562. doi: 10.1007/s10646-016-1614-1 CrossRefPubMedGoogle Scholar
  58. Wang CY, Zhou JW, Liu J, Du DL (2017) Responses of soil N-fixing bacteria communities to invasive species over a gradient of simulated nitrogen deposition. Ecol Eng 98:32–39. doi: 10.1016/j.ecoleng.2016.10.073 CrossRefGoogle Scholar
  59. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007b) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73:5261–5267. doi: 10.1128/AEM.00062-07 CrossRefGoogle Scholar
  60. Wang RL, Staehelin C, Dayan FE, Song YY, Su YJ, Zeng RS (2012) Simulated acid rain accelerates litter decomposition and enhances the allelopathic potential of the invasive plant Wedelia trilobata (creeping daisy). Weed Sci 60:462–467. doi: 10.1614/WS-D-12-00016.1 CrossRefGoogle Scholar
  61. Wang TJ, Jiang F, Li S, Liu Q (2007a) Trends in air pollution during 1996–2003 and cross-border transport in city clusters over the Yangtze River Delta Region of China. Terr Atmos Ocean Sci 5:995–1009. doi: 10.3319/TAO.2007.18.5.995(A) CrossRefGoogle Scholar
  62. Xie SY, Wang RB, Zheng HH (2012) Analysis on the acid rain from 2005 to 2011 in China. Environ Monit Forewarn 4:33–37 (In Chinese)Google Scholar
  63. Xu CW, Yang MZ, Chen YJ, Chen LM, Zhang DZ, Mei L, Shi YT, Zhang HB (2012) Changes in non-symbiotic nitrogen-fixing bacteria inhabiting rhizosphere soils of an invasive plant Ageratina adenophora. Appl Soil Ecol 54:32–38. doi: 10.1016/j.apsoil.2011.10.021 CrossRefGoogle Scholar
  64. Xu HQ, Zhang JE, Ouyang Y, Lin L, Quan GM, Zhao BL, Yu JY (2015) Effects of simulated acid rain on microbial characteristics in a lateritic red soil. Environ Sci Pollut R 22:18260–18266. doi: 10.1007/s11356-015-5066-6 CrossRefGoogle Scholar
  65. Yan XL, Liu QR, Shou HY, Zeng XF, Zhang Y, Chen L, Liu Y, Ma HY, Qi SY, Ma JS (2014) The categorization and analysis on the geographic distribution patterns of Chinese alien invasive plants. Biodivers Sci 22:667–676 (In Chinese)CrossRefGoogle Scholar
  66. Yang Y, Zhao WJ, Li ZH, Zhu SF (2011) Molecular identification of a ‘Candidatus Phytoplasma ziziphi’-related strain infecting Amaranth (Amaranthus retroflexus L.) in China. J Phytopathol 159:635–637. doi: 10.1111/j.1439-0434.2011.01808.x CrossRefGoogle Scholar
  67. Zhang YJ, Chang HR (2012) The impact of acid rain on China’s socioeconomic vulnerability. Nat Hazards 64:1671–1683. doi: 10.1007/s11069-012-0319-x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Institute of Environment and Ecology, Academy of Environmental Health and Ecological Security & School of the Environment and Safety EngineeringJiangsu UniversityZhenjiangPeople’s Republic of China

Personalised recommendations