Abstract
Bacteria are associated with the root system of plants in the endophytic and rhizospheric micro-habitats. In this paper, we used cultivation-independent methods to examine how the soil mercury contamination (present or absent) and the host plant species (Aeschynomene fluminensis and P. acuminatum) interfered with endophytic and rhizospheric bacterial communities in a humid area of the Pantanal biome. The capacity of the most abundant species to remediate the metal was assessed in cells immobilized on alginate spheres. The endophytic and rhizospheric communities were composed of respectively 22 and 26 phyla, 237 and 382 genera, and 644 and 3549 bacterial operational taxonomic units. The soil mercury contamination increased the alpha diversity indicators (p < 0.05, test T) only in the rhizospheric micro-habitat. The presence of the metal did not affect the beta diversity (composition and abundance) of endophytic bacteria (p < 0.05; ANOSIN), but differently influenced the interactions within endophytic and rhizospheric bacterial communities. The host species and the presence of the metal significantly altered the beta diversity of the rhizospheric communities (p < 0.05; ANOSIN). Arthrobacter defluvii_C11, Bacillus anthracis_C77, Pantoea_agglomerans_BacI11 and Acinetobacter_baumannii_BacI43 were immobilized on alginate beads, and removed more than 80% of the mercury in solution. Future studies are required to examine whether the endophytic environment acts as a buffer over other contaminants and reduces the impact of the metal on endophytic bacterial communities.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The NCBI access numbers to the raw NGS data are at BioProject: PRJNA613233 (SRR11344403 - SRR11344426).
References
Ankati S, Rani TS, Podile AR (2018) Changes in root exudates and root proteins in groundnut–Pseudomonas sp interaction contribute to root colonization by bacteria and defense response of the host. J Plant Growth Regul 38:523–538. https://doi.org/10.1007/s00344-018-9868-x
Betancur-Corredor B, Loaiza-Usuga JC, Denich M, Borgemeister C (2018) Gold mining as a potential driver of development in Colombia: challenges and opportunities. J Clean Prod 199:538–553. https://doi.org/10.1016/j.jclepro.2018.07.142
Castelino M, Eyre S, Moat J, Fox G, Martin P, Ho P, Upton M, Barton A (2017) Optimisation of methods for bacterial skin microbiome investigation: primer selection and comparison of the 454 versus MiSeq platform. BMC Microbiol 17(1):23. https://doi.org/10.1186/s12866-017-0927-4
Ceccatto AP, Testoni MC, Ignácio AR, Santos-Filho M, Malm O, Díez S (2016) Mercury distribution in organs of fish species and the associated risk in traditional subsistence villagers of the Pantanal wetland. Environ Geochem Health 38(3):713–722. https://doi.org/10.1007/s10653-015-9754-4
Chen Y, Jiang Y, Huang H, Mou L, Ru J, Zhao J, Xiao S (2019) Long-term and high-concentration heavy-metal contamination strongly influences the microbiome and functional genes in Yellow River sediments. Sci Total Environ 637–638:1400–1412. https://doi.org/10.1016/j.scitotenv.2018.05.109
Cheng D, Tian Z, Feng L, Xu L, Wang H (2019) Diversity analysis of the rhizospheric and endophytic bacterial communities of Senecio vulgaris L. (Asteraceae) in na invasive range. PeerJ 6:e6162. https://doi.org/10.7717/peerj.6162
Chi L, Bian X, Gao B, Tu P, Ru H, Lu K (2017) The effects of an environmentally relevant level of arsenic on the gut microbiome and its functional metagenome. Toxicol Sci 160:193–204. https://doi.org/10.1093/toxsci/kfx174
Chong J, Liu P, Zhou G, Xia J (2020) Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nature 15:799–821. https://doi.org/10.1038/s41596-019-0264-1
Cobo-Diaz JF, Baroncelli R, Le Floch G, Picot A (2019) Combined metabarcoding and co-occurrence network analysis to profile the bacterial, fungal and fusarium communities and their interactions in maize stalks. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00261
Cordero J, Freitas JR, Germida JJ (2020) Bacterial microbiome associated with the rhizosphere and root unterior of crops in Saskatchewan, Canada. Can J Microbiol 66(1):71–85. https://doi.org/10.1139/cjm-2019-0330
Courtois P, Rorat A, Lemiere S, Guyoneaud R, Attard E, Levard C, Vandenbulcke F (2019) Ecotoxicology of silver nanoparticles and their derivatives introduced in soil with or without sewage sludge: a review of effects on microorganisms, plants and animals. Environ Pollut 253:578–598. https://doi.org/10.1016/j.envpol.2019.07.053
Debroas D, Domaizon I, Humbert JF, Jardillier L, Lepère C, Oudart A, Taïb N (2017) Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiol Ecol 93. https://doi.org/10.1093/femsec/fix023
Deng L, Zeng G, Fan C, Lu L, Chen X, Chen M, Wu H, He X, He Y (2015) Response of rhizosphere microbial community structure and diversity to heavy metal co-pollution in arable soil. Appl Microbiol Biotechnol 99:8259–8269. https://doi.org/10.1007/s00253-015-6662-6
Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113. https://doi.org/10.1186/1471-2105-13-113
Dhariwal A, Chong J, Habib S, King I, Agellon LB, Xia J (2017) MicrobiomeAnalyst - a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188. https://doi.org/10.1093/nar/gkx295
Dessaux Y, Grandclément C, Faure D (2016) Engineering the rhizosphere. Trends Plant Sci 21(3):266–278. https://doi.org/10.1016/j.tplants.2016.01.002
Ding Z, Wu J, You A, Huang B, Cao C (2016) Effects of heavy metals on soil microbial community structure and diversity in the rice (Oryza sativa L. subsp. japonica, food crops Institute of Jiangsu Academy of agricultural sciences) rhizosphere. J. Soil Sci. Plant Nutr 63(1):75–83. https://doi.org/10.1080/00380768.2016.1247385
Dixit R, Wasiullah MD, Pandiyan K, Singh BU, Sahu A, Shukla R, Singh BP, Rai JP, Sharma KP, Lade H, Paul DB (2015) Biorremediation of heavy metals from soil and aquatic enrivonment: no overview of principles and criteria of fundamental processes. Sustainability 7:2189–2212. https://doi.org/10.3390/su7022189
Dissanayake AJ, Purahong W, Wubet T, Hyde KD, ZhangW XH, Zhang G, Fu C, Liu M, Xing Q, Li X, Yan J (2018) Direct comparison of culture-dependent and culture-independent molecular approaches reveal the diversity of fungal endophytic communities in stems of grapevine (Vitis vinifera). Fungal Divers 90:85–107. https://doi.org/10.1007/s13225-018-0399-3
Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2019) PICRUSt2: an improved and customizable approach for metagenome inference. bioRxiv preprint. https://doi.org/10.1101/672295
Dunnett C, Tamhane AC (1991) Step-down multiple tests for comparing treatments with a control in unbalanced one-way layouts. Stat Med 10:939–947. https://doi.org/10.1002/sim.4780100614
Edgar RC (2010) Usearch. United States: N. p. Web
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. J Bioinform 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Edwards JE, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S (2015) Structure, variation, and assembly of the root associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920. https://doi.org/10.1073/pnas.1414592112
Franchi E, Agazzi G, Rolli E, Borin S, Marasco R, Chiaberge S, Conte A, Filtri P, Pedron F, Rosellini I, Barbafieri M, Petruzzelli G (2016) Exploiting hydrocarbon-degrading indigenous bacteria for bioremediation and phytoremediation of a multicontaminated soil. Chem Eng Technol 39(9):1676–1684. https://doi.org/10.1002/ceat.201500573
Frossard A, Hartmann M, Frey B (2017) Tolerance of the forest soil microbiome to increasing mercury concentrations. Soil Biol Biochem 105:162–176. https://doi.org/10.1016/j.soilbio.2016.11.016
Frossard A, Donhauser J, Mestrot A, Gygax S, Baath E, Frey B (2018) Long- and short-term effects of mercury pollution on the soil microbiome. Soil Biol Biochemi 120:191–199. https://doi.org/10.1016/j.soilbio.2018.01.028
Gaiero JR, McCall C, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100(9):1738–1750. https://doi.org/10.3732/ajb.1200572
Giovanella P, Cabral L, Costa AP, Camargo FAO, Gianello C, Bento FM (2017) Metal resistance mechanisms in gran-negative bactéria and their potential to remove hg in the presence of other metals. Ecotoxicol Environ Saf 140:162–169. https://doi.org/10.1016/j.ecoenv.2017.02.010
Gong X, Huang D, Liu Y, Zeng G, Wang R, Wei J, Huang C, Xu P, Wan J, Zhang C (2018) Pyrolysis and reutilization of plant residues after phytoremediation of heavy metals contaminated sediments: for heavy metals stabilization and dye adsorption. Bioresour Technol 253:64–71. https://doi.org/10.1016/j.biortech.2018.01.018
Gu B, Lu X, Johs A, Pierce EM (2019) Mercury in water. Encyclopedia Water: Sci, Technol, Soc. https://doi.org/10.1002/9781119300762.wsts0001
Guo J, Muhammad H, Lv X, Wei T, Ren X, Jia H, Atif S, Hua L (2020) Prospects and applications of plant growth promoting rhizobacteria to mitigate soil metal contamination: a review. Chemosphere 246:125823. https://doi.org/10.1016/j.chemosphere.2020.125823
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):4–9
Hardoim PR, Overbeek LSV, Berg G, Pirtilla AM, Compant S, Campisano A, Doring M, Sessitisch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. mBio 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Hill MO (1973) Diversity and evenness: a unifying notation and its consequence. Ecology 54(2):427–432. https://doi.org/10.2307/1934352
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2015) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462. https://doi.org/10.1093/nar/gkv1070
Kim JO, Lee YW, Chung J (2013) The role of organic acids in the mobilization of heavy metals from soil. KSCE J Civ Eng 17:1596–1602. https://doi.org/10.1007/s12205-013-0323-z
Kiyono M, Pan-Hou H (1999) The merG gene product is involved in phenylmercury resistance in Pseudomonas strain K-62. J Bacteriol 81:726–730
Kiran MG, Parkshirajan K, Das G (2018) Heavy metal removal from aqueous solution using sodium alginate immobilized sulfate reducing bacteria: mechanism and process optimization. Environ Manag Today 218:486–496. https://doi.org/10.1016/j.jenvman.2018.03.020
Klimek B, Sitarz A, Choczyński M, Niklińska M (2016) The effects of heavy metals and total petroleum hydrocarbons on soil bacterial activity and functional diversity in the upper Silesian industrial region (Poland). Water Air Soil Pollut 227. https://doi.org/10.1007/s11270-016-2966-0
Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484. https://doi.org/10.1111/j.1365-2672.2010.04670.x
Lawrence E (2000) Microbial mercury mop. Nature. https://doi.org/10.1038/news000106-8
Li X, Meng D, Li J, Yin H, Liu H, Liu X, Cheng C, Xiao Y, Liu Z, Yan M (2017) Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environ Pollut 231:908–917. https://doi.org/10.1016/j.envpol.2017.08.057
Ling L, Ma W, Li Z, Jiao Z, Xu X, Lu L, Zhang X, Feng J, Zhang J (2020) Comparative study of the endophytic and rhizospheric bacterial diversity of Angelica sinensis in three main producing areas in Gansu. China S Afr J Bot 134:36–42. https://doi.org/10.1016/j.sajb.2019.12.029
Lionaki E, Tavernarakis N (2013) Assessing aging and senescent decline in Caenorhabditis elegans: cohort survival analysis. Methods Mol Biol 965:473–484. https://doi.org/10.1007/978-1-62703-239-1_31
Liotti RG, Figueiredo MIS, Silva GF, Mendonça EAF, Soares MA (2018) Diversity of cultivable bacterial endophytes in Paullinia cupana and their potential for plant growth promotion and phytopathogen control. Microbiol Res 207:8–18. https://doi.org/10.1016/j.micres.2017.10.011
Liotti RG, Figueiredo MIS, Soares MA (2019) Streptomyces griseocarneus R132 controls phytopathogens and promotes growth of pepper (Capsicum annuum). Biocontrol 138:104065. https://doi.org/10.1016/j.biocontrol.2019.104065
Li X, Meng D, Li J, Yin H, Liu H, Liu X, Cheng C, Xiao Y, Liu Z, Yan M (2017b) Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environ Pollut 231:908–917. https://doi.org/10.1016/j.envpol.2017.08.057
Liu SH, Zeng GM, Niu QY, Liu Y, Zhou L, Jiang LH, Tan X, Xuv P, Zhang C, Cheng M (2017) Bioremediation mechanisms of combined pollution of PAHs and heavy metals by bacteria and fungi: a mini review. Bioresour Technol 224:25–33. https://doi.org/10.1016/j.biortech.2016.11.095
Lu L, Yin S, Liu X, Zhang W, Gu T, Shen Q, Qiu H (2013) Fungal networks in yield-invigorating and-debilitating soils induced by prolonged potato monoculture. Soil Biol Biochem 65:186–194. https://doi.org/10.1016/j.soilbio.2013.05.025
Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25. https://doi.org/10.1016/j.jenvman.2016.02.047
Mahbub KR, Bahar MM, Labbate M, Labbate M, Krishnan K, Andrews S, Naidu R, Megharaj M (2017) Bioremediation of mercury: not properly exploited in contaminated soils! Appl Microbiol Biotechnol 101:963–976. https://doi.org/10.1007/s00253-016-8079-2
Mahmoud MS, Mohamed SA (2017) Calcium alginate as an eco-friendly supporting material for Baker’s yeast strain in chromium bioremediation. HBRC J 13(3):245–254. https://doi.org/10.1016/j.hbrcj.2015.06.003
Mariano C, Mello IS, Barros BM, Silva GF, Terezo AJ, Soares MA (2020) Mercury alters the rhizobacterial community in Brazilian wetlands and it can be bioremediated by the plant-bacteria association. Environ Sci Pollut Res 27:13550–13564. https://doi.org/10.1007/s11356-020-07913-2
Mello IS, Pietro-Souza W, Barros BM, Silva GF, Campos ML, Soares MA (2019) Endophytic bacteria mitigate mercury toxicity to host plants. Symbiosis 79:251–262. https://doi.org/10.1007/s13199-019-00644-0
Mgbemene CA, Nnaji CC, Nwozor C (2016) Industrialization and its backlash: focus on climate change and its consequences. Environ Sci Technol 9:301–316. https://doi.org/10.3923/jest.2016.301.316
Moronta-Barrios F, Gionechetti F, Pallavicini A, Marys E, Venturi V (2018) Bacterial microbiota of rice roots: 16S-based taxonomic profiling of endophytic and rhizospheric diversity, endophytes isolation and simplified endophytic community. Microorganisms 6. https://doi.org/10.3390/microorganisms6010014
Nair D, Padmavathy S (2014) Impact of endophytic microorganisms on plants, rnvironment and humans. Sci World J 2014:1–11. https://doi.org/10.1155/2014/250693
Oksanen J, Blanchet FG, Friendly F, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Package ‘vegan’ https://cran.r-project.org, https://github.com/vegandevs/vegan
Olesen JM, Bascompte J, Dupont YL, Jordano P (2006) The smallest of all worlds: pollination networks. J Theor Biol 240:270–276. https://doi.org/10.1016/j.jtbi.2005.09.014
Olivero-Verbel J, Carranza-Lopez L, Caballero-Gallardo K, Ripoll-Arboleda A, Muñoz-Sosa D (2016) Human exposure and risk assessment associated with mercury pollution in the Caqueta River, Colombian Amazon. Environ Sci Pollut Res 23(20):20761–20771. https://doi.org/10.1007/s11356-016-7255-3
Parajuli A, Grönroos M, Kauppi S, Plociniczak T, Roslund MI, Galitskaya P, Laitinen OH, Hyoty H, Jumpponen A, Strömmer R, Romantschuk M, Hui N, Sinkkonen A (2017) The abundance of health-associated bacteria is altered in PAH polluted soils—implications for health in urban areas? PLoS One 12:e0187852. https://doi.org/10.1371/journal.pone.0187852
Parlapania FF, Michailidouc S, Pasentsis K, Argiriou A, Kreya G, Boziaris IS (2018) A meta-barcoding approach to assess and compare the storage temperature-dependent bacterial diversity of gilt-head sea bream (Sparus aurata) originating from fish farms from two geographically distinct areas of Greece. Int J Food Microbiol 278:36–43. https://doi.org/10.1016/j.ijfoodmicro.2018.04.027
Pei C, Mi C, Sun L, Liu W, Li O, Hu X (2016) Diversity of endophytic bacteria of Dendrobium officinale based on culture-dependent and culture-independent methods. Biotechnol Biotechnol Equip 31(1):112–119. https://doi.org/10.1080/13102818.2016.1254067
Pietro-Souza W, Pereira FC, Mello IS, Stachack FFF, Terezo AJ, Cunha CN, White JF, Li H, Soares MA (2020) Mercury resistance and bioremediation mediated by endophytic fungi. Chemosphere 240:124874. https://doi.org/10.1016/j.chemosphere.2019.124874
Pietro-Souza W, Mello IS, Vendruscullo SJ, Silva GFD, Cunha CND, White JF, Soares MA (2017) Endophytic fungal communities of Polygonum acuminatum and Aeschynomene fluminensis are influenced by soil mercury contamination. PLoS One 12:e0182017. https://doi.org/10.1371/journal.pone.0182017
Porta-de-la-Riva M, Fontrodona L, Villanueva A, Cerón J (2012) Basic Caenorhabditis elegans methods: synchronization and observation. J Vis Exp. https://doi.org/10.3791/4019
Prashar P, Kapoor N, Sachdeva S (2013) Rhizosphere: its structure, bacterial diversity and significance. Rev Environ Sci Biotechnol 13:63–77. https://doi.org/10.1007/s11157-013-9317-z
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rahman Z, Singh VP (2018) Assessment of heavy metal contamination and hg-resistant bacteria in surface water from different regions of Delhi. Saudi J Biol Sci 25(8):1687–1695. https://doi.org/10.1016/j.sjbs.2016.09.018
Roberts DW (2019) Labdsv: ordination and multivariate analysis for ecology. R package version 2.0–1. https://CRAN.R-project.org/package=labdsv
Sánchez-López AS, Thijs S, Beckers B, González-Chávez C, Weyens N, Carrilo-Gonzáles R, Vangrosveld J (2017) Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues. Plant Soil 422:51–66. https://doi.org/10.1007/s11104-017-3176-2
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2500. https://doi.org/10.1101/gr.1239303
Shashidhar R, Kumar SA, Misra HS, Bandekar JR (2010) Evaluation of the role of enzymatic and nonenzymatic antioxidant systems in the radiation resistance of Deinococcus. Can J Microbiol 56(3):195–201
Sinha A, Pant KK, Khare KS (2012) Studies on mercury bioremediation by alginate immobilized mercury tolerant Bacillus cereus cells. Int Biodeterior Biodegradation 71:1–8. https://doi.org/10.1016/j.ibiod.2011.12.014
Song W, Wang Y, Li T, Liu D, Zhu M, Zhao Z (2018) Host specificity determines the assemblage of root endophytic bacteria of plants growing in metal contaminated soil. PeerJ Preprints. https://doi.org/10.7287/peerj.preprints.27143v1
Sun W, Xiong Z, Chu L, Li W, Soares MA, White JJF, Li H (2019) Bacterial communities of three plant species from Pb-Zn contaminated sitesand plant-growth promotional benefits of endophytic Microbacteriumsp. (strain BXGe71). J Hazrd Mater 370:225–331. https://doi.org/10.1016/j.jhazmat.2018.02.003
Tian B, Hua YJ (2010) Carotenoid biosynthesis in extremophilic Deinococcus–Thermus bacteria. Trends Microbiol 18(11):512–520. https://doi.org/10.1016/j.tim.2010.07.007
Tian HJ, Feng J, Zhang LM, He JZ, Liu YR (2020) Ecological drivers of methanotrophic communities in paddy soils around mercury mining áreas. Sci Total Environ 721:137760. https://doi.org/10.1016/j.scitotenv.2020.137760
Tipayno SC, Truu J, Samaddar S, Truu M, Preem JK, Oopkaup K, Epenberg M, Chatterjee P, Kang Y, Kim K, Sa T (2018) The bacterial community structure and functional profile in the heavy metal contaminated paddy soils, surrounding a nonferrous smelter in South Korea. Ecol Evol 8(12):6157–6168. https://doi.org/10.1002/ece3.4170
Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21(3):187–198. https://doi.org/10.1016/j.tplants.2016.01.005
Verma SK, Kharwar RN, White JF (2019) The role of seed-vectored endophytes in seedling development and establishment. Symbiosis 78:107–113
Wang YD, Greger M (2004) Clonal differences in mercury tolerance, accumulation, and distribution in willow. J Environ Which 33:1779–1785. https://doi.org/10.2134/jeq2004.1779
White JF, Kingsley KL, Butterworth S, Brindisi L, Gatei JW, Elmore MT, et al. 2019. Seed vectored microbes: their roles in improving seedling fitness and competitor plant suppression. In seed endophytes; Verma, S. K., White J. F. Jr., (eds) Cham: springer: pp. 823 3-20
Xue N, Wang L, Li W, Wnag S, Pan X, Zhang D (2020) Increased inheritance of structure and function of bacterial communities and pathogen propagation in plastisphere along a river with increasing antibiotics pollution gradiente. Environ Pollut 265:114641. https://doi.org/10.1016/j.envpol.2020.114641
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRna gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio. 2. https://doi.org/10.1128/mBio.00122-11
Funding
This work was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grant # 409062/2018–9), Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT, grant # 568258/2014) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Not applicable
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 732 kb)
Rights and permissions
About this article
Cite this article
da Silva Maciel, J.H., Mello, I.S., Vendrusculo, S.J. et al. Endophytic and rhizospheric bacterial communities are affected differently by the host plant species and environmental contamination. Symbiosis 85, 191–206 (2021). https://doi.org/10.1007/s13199-021-00804-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-021-00804-1