Abstract
Copper mining caused severe damage to the ecological environment of mining areas. The combination of microbe and plant remediation has an application potential in improving the absorption and transformation efficiency of heavy metals. The phyllosphere is the largest biointerface on the planet, and bacteria are the dominant microbial inhabitants of the phyllosphere, believed to be critical to plant growth and health. This study investigated the phyllospheric and soil bacteria communities using high-throughput sequencing, and endophyte infection statuses of four natural grasses by toluidine blue heparin assay. Results showed variation in phyllospheric bacterial community structure. Gammaproteobacteria were the most abundant bacterial population. Bacilli were found in the phyllosphere of Bothriochloa ischaemum and Imperata cylindrica, while Clostridia were only found in Calamagrostis epigejos. Alphaproteobacteria were the dominant bacteria in soil. In addition, bacterial communities were influenced by endophytic infection statuses. Oxalobacteraceae was associated with soil carbon and sulfur. Enterobacteriaceae had negative correlation with the ratio of soil carbon and nitrogen, and had positive correlation with Cd content. These results offer useful insights into phyllospheric bacterial community variance in four different natural grasses in a copper tailings dam.
This is a preview of subscription content, access via your institution.



References
Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3(4):267–274
Bálint M, Tiffin P, Hallström B, O Hara RB, Olson MS, Fankhauser JD et al (2013) Host genotype shapes the foliar fungal microbiome of Balsam Poplar (Populus balsamifera). PloS ONE 8(1):e53987
Balintkurti P, Simmons SJ, Blum JE, Ballaré CL, Stapleton AE (2010) Maize leaf epiphytic bacteria diversity patterns are genetically correlated with resistance to fungal pathogen infection. Mol Plant Microbe Interact 23(4):473–484
Chinnadurai C, Balachandar D, Sundaram SP (2009) Characterization of 1-aminocyclopropane-1-carboxylate deaminase producing methylobacteria from phyllosphere of rice and their role in ethylene regulation. World J Microbiol Biotechnol 25(8):1403–1411
Compant S, Heijden MGAV, Sessitsch A (2010) Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiol Ecol 73(2):197–214
Conesa HM, Faz A, Arnaldos R (2007) Initial studies for the phytostabilization of a mine tailing from the Cartagena-La Union mining district (SE Spain). Chemosphere 66(1):38–44
Costa DMD, Samarasinghe SST, Dias HRD, Dissanayake DMN (2008) Control of rice sheath blight by phyllosphere epiphytic microbial antagonists. Phytoparasitica 36(1):52–65
Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato YI, Morisaki H et al (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46(3):617–629
He Z, Xie X, Xiao S, Liu J, Qiu G (2010) Microbial diversity of mine water at Zhong Tiaoshan copper mine, China. J Basic Microbiol 47(6):485–495
Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Appl Environ Microbiol 76(24):8117–8125
Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70(5):2667
Ikeda S, Tokida T, Nakamura H, Sakai H, Usui Y, Okubo T et al (2015) Characterization of leaf blade- and leaf sheath-associated bacterial communities and assessment of their responses to environmental changes in CO2, temperature, and nitrogen levels under field conditions. Microbes Environ 30(1):51–62
Janarthine SRS, Eganathan P (2012) Plant growth promoting of endophytic sporosarcina aquimarina SjAM16103 isolated from the pneumatophores of Avicennia marina L. Int J Microbiol 2012(4):532060
Jennifera R, Samuel O (2010) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97(2):247–255
Jia T, Oberhofer M, Shymanovich T, Faeth SH (2016) Effects of hybrid and non-hybrid Epichloë endophytes and their associated host genotypes on the response of a native grass to varying environments. Microb Ecol 72(1):185–196
Lindow SE, Andersen GL (1996) Influence of immigration on epiphytic bacterial populations on navel orange leaves. Appl Environ Microbiol 62(8):2978–2987
Lipson DA, Murthy R (2006) Relationships between microbial community structure and soil processes under elevated atmospheric carbon dioxide. Microbe Ecol 51(3):302–314
Mano H, Tanaka F, Nakamura C, Kaga H, Morisaki H (2007) Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 22(22):175–185
Mirzahosseini Z, Shabani L, Sabzalian MR, Sharifi-Tehrani M (2014) Neotyphodium endophytes may increase tolerance to Ni in tall fescue. Eur J Soil Biol 63:33–40
Morris CE, Lucotte T (1993) Dynamics and variability of bacterial population density on leaves of field-grown endive destined for ready-to-use processing. Int J Food Sci Tech 28(2):201–209
Oberhofer M, Güsewell S, Leuchtmann A (2014) Effects of natural hybrid and non-hybrid Epichloë endophytes on the response of Hordelymus europaeus to drought stress. New Phytol 201(1):242–253
Okubo T, Tokida T, Ikeda S, Bao Z, Tago K, Hayatsu M et al (2014) Effects of elevated carbon dioxide, elevated temperature, and rice growth stage on the community structure of rice root-associated bacteria. Microbes Environ 29(2):184–190
Osono T (2014) Diversity and ecology of endophytic and epiphytic fungi of tree leaves in Japan: a review. Springer, New Delhi, pp 3–26
Peñuelas J, Rico L, Ogaya R, Jump AS, Terradas J (2012) Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biology 14(4):565–575
Rasche F, Sessitsch A (2006) Structural characteristics and plant-beneficial effects of bacteria colonizing the shoots of field grown conventional and genetically modified T4-lysozyme producing potatoes. Plant Soil 289(1):123–140
Rasche F, Trondl R, Naglreiter C, Reichenauer TG, Sessitsch A (2006) Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can J Microbiol 52(11):1036
Ren G, Zhang H, Lin X, Zhu J, Jia Z (2015) Response of leaf endophytic bacterial community to elevated CO2 at different growth stages of rice plant. Front Microbiol 6:855
Ren G, Zhu C, Alam MS, Tokida T, Sakai H, Nakamura H et al (2015) Response of soil, leaf endosphere and phyllosphere bacterial communities to elevated CO2 and soil temperature in a rice paddy. Plant Soil 392(1):27–44
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340–1351
Rudgers JA, Clay K (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol Rev 21(2):107–124
Saari S, Faeth SH (2012) Hybridization of Neotyphodium endophytes enhances competitive ability of the host grass. New Phytol 195(1):231–236
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75(23):7537–7541
Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica) 90(4):569–578
Sievert SM, Kiene RP, Schultz-Vogt HN (2007) The sulfur cycle. Oceanography 20(2):117–123
Tong J, Miaowen C, Juhui J, Jinxian L, Baofeng C (2017) Endophytic fungi and soil microbial community characteristics over different years of phytoremediation in a copper tailings dam of Shanxi, China. Sci Total Environ 574:881–888
Wang R, Jia T, Cao M, Chai B (2018) Characteristics of soil physicochemical properties and enzyme activities over different characteristics of soil physicochemical properties and enzyme activities over different reclaimed years in a copper tailings dam. Environ Sci 39(07):3339–3348
Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105(6):1744–1755
Xiong XQ, Liao HD, Ma JS, Liu XM, Zhang LY, Shi XW et al (2014) Isolation of a rice endophytic bacterium, Pantoea sp. Sd-1, with ligninolytic activity and characterization of its rice straw degradation ability. Lett Appl Microbiol 58(2):123–129
Yang CH, Crowley DE, Borneman J, Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci USA 98(7):3889–3894
Zamani N, Sabzalian MR, Khoshgoftarmanesh A, Afyuni M (2015) Neotyphodium endophyte changes phytoextraction of zinc in Festuca arundinacea and Lolium perenne. Int J Phytoremediat 17(5):456–463
Zhang W, Xu J, Zhang T (2005) Advancement on soil fungal research. J Fungal Res 3:56–62
Zhou Y, Li X, Qin J, Liu H, Chen W, Niu Y et al (2016) Effects of simultaneous infections of endophytic fungi and arbuscular mycorrhizal fungi on the growth of their shared host grass Achnatherum sibiricum under varying N and P supply. Fungal Ecol 20:56–65
Acknowledgements
This work was supported by the National Natural Science Foundation of China under Grant No. 31600308, Shanxi Scholarship Council of China under Grant No. 2016-006, and Shanxi Province Science Foundation for Youths under Grant No. 201601D021101.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jia, T., Wang, RH. & Chai, BF. Various Phyllosphere and Soil Bacterial Communities of Natural Grasses and the Impact Factors in a Copper Tailings Dam. Curr Microbiol 76, 7–14 (2019). https://doi.org/10.1007/s00284-018-1575-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-018-1575-0