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Urban traffic changes the biodiversity, abundance, and activity of phyllospheric nitrogen-fixing bacteria

  • Yang Li
  • Hong Sun
  • Zhaojun Wu
  • Hui Li
  • Qingye SunEmail author
Research Article

Abstract

The phyllosphere provides appropriate conditions for colonization by microorganisms, including diazotrophic bacteria. However, a poor understanding of the effects of the atmospheric environment on the phyllospheric diazotrophic communities persists. We detected the biodiversity, abundance, and activity of nitrogen-fixing bacteria in the phyllospheres of two evergreen shrubs, Nerium indicum Mill. and Osmanthus sp., sampled from urban areas with heavy traffic, a college campus, and a forest. Quantitative PCR analysis indicated that the copy numbers of nifH sequences were highest in the phyllospheres of both plants in heavy-traffic urban areas and correlated with the recorded nitrogenase activities of the phyllospheres. Similarly, the phyllosphere from heavy-traffic urban areas also possessed the highest biodiversity indices of diazotrophic communities from both the two plants. Pyrosequencing analysis revealed a diversity of nifH sequences in phyllosphere that were mostly uniquely found in the phyllosphere, and many of these were proteobacteria-like and cyanobacteria-like. Members of the Proteobacteria, mostly of which were not closely related to unknown organisms, were detected exclusively in the phyllosphere and represented substantial fractions of their associated diazotrophic communities. Our study provides initial insight into the shifts in the biodiversity and community structure of N2-fixing microorganisms in the phyllospheres of different atmospheric environments.

Keywords

Atmospheric environment Phyllosphere Pyrosequencing nifH gene 

Notes

Acknowledgments

Thanks for the subsidization by the Personnel Training Project of the Mining Environmental Restoration and Wetlands Ecological Security Collaborative Innovation Center, Anhui University.

Funding

This work was supported by the PhD research startup foundation of Anhui University (J01003269).

Supplementary material

11356_2019_5008_MOESM1_ESM.doc (872 kb)
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11356_2019_5008_MOESM2_ESM.xls (127 kb)
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11356_2019_5008_MOESM3_ESM.xls (91 kb)
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References

  1. Abril AB, Torres PA, Bucher EH (2005) The importance of phyllosphere microbial populations in nitrogen cycling in the Chaco semi-arid woodland. J Trop Ecol 21:103–107CrossRefGoogle Scholar
  2. Agawin NSR, Ferriol P, Sintes E, Moyà G (2017) Temporal and spatial variability of in situ nitrogen fixation activities associated with the Mediterranean seagrass Posidonia oceanica meadows. Limnol Oceanogr 62:2575–2592CrossRefGoogle Scholar
  3. Balasooriya BLWK, Samson R, Mbikwa F, Vitharana UWA, Boeckx P, Van Meirvenne M (2009) Biomonitoring of urban habitat quality by anatomical and chemical leaf characteristics. Environ Exp Bot 65:386–394CrossRefGoogle Scholar
  4. Bentley BL, Carpenter EJ (1984) Direct transfer of newly-fixed nitrogen from free-living epiphyllous microorganisms to their host plant. Oecologia 63:52–56CrossRefGoogle Scholar
  5. Bodenhausen N, Bortfeldmiller M, Ackermann M, Vorholt JA (2014) A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet 10:e1004283CrossRefGoogle Scholar
  6. Brighigna L, Gori A, Gonnelli S, Favilli F (2000) The influence of air pollution on the phyllosphere microflora composition of Tillandsia leaves (Bromeliaceae). Rev Biol Trop 48:511–517Google Scholar
  7. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106:16428–16433CrossRefGoogle Scholar
  8. Ferguson DK (2008) Biology of the plant cuticle. Syst Bot 33:613CrossRefGoogle Scholar
  9. Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S (2011) Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl Environ Microbiol 77:7647–7655CrossRefGoogle Scholar
  10. Finkel OM, Burch AY, Elad T, Huse SM, Lindow SE, Post AF, Belkin S (2012) Distance-decay relationships partially determine diversity patterns of phyllosphere bacteria on Tamarix trees across the Sonoran Desert. Appl Environ Microbiol 78:6187–6193CrossRefGoogle Scholar
  11. Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A (2008) Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:561–570CrossRefGoogle Scholar
  12. Hamisi M, Díez B, Lyimo T, Ininbergs K, Bergman B (2013) Epiphytic cyanobacteria of the seagrass Cymodocea rotundata: diversity, diel nifH expression and nitrogenase activity. Environ Microbiol Rep 5:367–376CrossRefGoogle Scholar
  13. Hsu S-F, Buckley DH (2009) Evidence for the functional significance of diazotroph community structure in soil. ISME J 3:124–136CrossRefGoogle Scholar
  14. Jacquot A, Li Z, Gojon A, Schulze W, Lejay L (2017) Post-translational regulation of nitrogen transporters in plants and microorganisms. J Exp Bot 68:2567–2580CrossRefGoogle Scholar
  15. Kardel F, Wuyts K, Maher BA, Samson R (2012) Intra-urban spatial variation of magnetic particles: monitoring via leaf saturation isothermal remanent magnetisation (SIRM). Atmos Environ 55:111–120CrossRefGoogle Scholar
  16. Liao W, Menge DNL, Lichstein JW, Ángeles-Pérez G (2017) Global climate change will increase the abundance of symbiotic nitrogen-fixing trees in much of North America. Glob Chang Biol 23:4777–4787CrossRefGoogle Scholar
  17. Orr CH, James A, Leifert C, Cooper JM, Cummings SP (2011) Diversity and activity of free-living nitrogen-fixing bacteria and total bacteria in organic and conventionally managed soils. Appl Environ Microbiol 77:911–919CrossRefGoogle Scholar
  18. Papen H, Gessler A, Zumbusch E, Rennenberg H (2002) Chemolithoautotrophic nitrifiers in the phyllosphere of a spruce ecosystem receiving high atmospheric nitrogen input. Curr Microbiol 44:56–60CrossRefGoogle Scholar
  19. 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 Microbiol 67:2255–2262CrossRefGoogle Scholar
  20. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JHJ (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6:1812–1822CrossRefGoogle Scholar
  21. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893CrossRefGoogle Scholar
  22. Reed SC, Cleveland CC, Townsend AR (2008) Tree species control rates of free-living nitrogen fixation in a tropical rain forest. Ecology 89:2924–2934CrossRefGoogle Scholar
  23. Reed SC, Townsend AR, Cleveland CC, Nemergut DR (2010) Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 164:521–531CrossRefGoogle Scholar
  24. Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139–144CrossRefGoogle Scholar
  25. Rico L, Ogaya R, Terradas J, Peñuelas J (2014) Community structures of N2-fixing bacteria associated with the phyllosphere of a Holm oak forest and their response to drought. Plant Biol 16:586–593CrossRefGoogle Scholar
  26. Rigonato J, Alvarenga DO, Andreote FD, Dias ACF, Melo IS, Kent A, Fiore MF (2012) Cyanobacterial diversity in the phyllosphere of a mangrove forest. FEMS Microbiol Ecol 80:312–322CrossRefGoogle Scholar
  27. Silva AFD, Freitas ADSD, Costa TL, Fernandes-Júnior PI, Martins LMV, Menezes KAS (2017) Biological nitrogen fixation in tropical dry forests with different legume diversity and abundance. Nutr Cycl Agroecosyst 107:321–334 1–14CrossRefGoogle Scholar
  28. Smets W, Wuyts K, Oerlemans E, Wuyts S, Denys S, Samson R, Lebeer S (2016) Impact of urban land use on the bacterial phyllosphere of ivy (Hedera sp.). Atmos Environ 147:376–383CrossRefGoogle Scholar
  29. Thuler DS, Floh EIS, Handro W, Barbosa HR (2003) Beijerinckia derxii releases plant growth regulators and amino acids in synthetic media independent of nitrogenase activity. J Appl Microbiol 95:799–806CrossRefGoogle Scholar
  30. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45CrossRefGoogle Scholar
  31. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840CrossRefGoogle Scholar
  32. Wanek W, Pörtl K (2005) Phyllosphere nitrogen relations: reciprocal transfer of nitrogen between epiphyllous liverworts and host plants in the understorey of a lowland tropical wet forest in Costa Rica. New Phytol 166:577–588CrossRefGoogle Scholar
  33. Wuytack T, Samson R, Wuyts K, Adriaenssens S, Kardel F, Verheyen K (2013) Do leaf characteristics of white willow (Salix alba L.), northern red oak (Quercus rubra L.), and scots pine (Pinus sylvestris L.) respond differently to ambient air pollution and other environmental stressors? Water Air Soil Pollut 224:1–14Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yang Li
    • 1
  • Hong Sun
    • 2
  • Zhaojun Wu
    • 1
  • Hui Li
    • 1
  • Qingye Sun
    • 1
    Email author
  1. 1.School of Resources and Environmental EngineeringAnhui UniversityHefeiChina
  2. 2.College of Life ScienceNortheast Forestry UniversityHarbinChina

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