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Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues

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Abstract

Aims

We investigated the possible transgenerational transfer of bacterial seed endophytes across three consecutive seed generations of Crotalaria pumila growing on a metal mining site in Mexico.

Methods

Seeds were collected during three successive years in the semi-arid region of Zimapan, Mexico. Total communities of seed endophytes were investigated using DNA extraction from surface sterilized seeds and 454 pyrosequencing of the V5-V7 hypervariable regions of the 16S rRNA gene.

Results

The communities consisted of an average of 75 operational taxonomic units (OTUs); richness and diversity did not change across years. Methylobacterium, Staphylococcus, Corynebacterium, Propionibacterium and eight other OTUs constituted >60% of the community in each generation. The microbiome was dominated by Methylobacterium (present in >80% of samples). Functions associated with the microbiome were C and N fixation, oxidative phosphorylation and photosynthesis activity.

Conclusions

The bacterial endophytic communities were similar across three consecutive seed generations. Among the core microbiome Methylobacterium strains were the most abundant and they can contribute to nutrient acquisition, plant growth promotion and stress resilience to their host in metal contaminated mine residues. Identification of the seed microbiome of C. pumila may lead to novel and more efficient inoculants for microbe-assisted phytoremediation.

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References

  • Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362. doi:10.1016/j.tibtech.2007.05.005

    Article  CAS  PubMed  Google Scholar 

  • Beckers B, Op de Beeck M, Thijs S, Truyens S, Weyens N, Boerjan W, Vangronsveld J (2016) Performance of 16 s RNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Front Microbiol 7:650. doi:10.3389/fmicb.2016.00650

    Article  PubMed  PubMed Central  Google Scholar 

  • Berg G, Rybakova D, Grube M, Köberl M (2015) The plant microbiome explored: implications for experimental botany. J Exp Bot erv466. doi: 10.1093/jxb/erv466

  • Bertalan M, Albano R, de Pádua V, Rouws L, Rojas C, Hemerly A et al (2009) Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics 10:450. doi:10.1186/1471-2164-10-450

    Article  PubMed  PubMed Central  Google Scholar 

  • Bibian AJ, Rudgers JA, Miller TE (2016) The role of host demographic storage in the ecological dynamics of heritable symbionts. Am Nat 188:446–459. doi:10.5061/dryad.54rv6

    Article  PubMed  Google Scholar 

  • Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:356329. doi:10.1371/journal.pone.0056329

    Article  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. doi:10.1146/annurev-arplant-050312-120106

    Article  CAS  PubMed  Google Scholar 

  • Burch AY, Do PT, Sbodio A, Suslow TV, Lindow SE (2016) High-level culturability of epiphytic bacteria and frequency of biosurfactant producers on leaves. Appl Environ Microb 82:5997–6009. doi:10.1128/AEM.01751-16

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al (2010a) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010b) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. doi:10.1093/bioinformatics/btp636

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Luo S, Xiao X, Guo H, Chen J, Wan Y et al (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46:383–389. doi:10.1016/j.apsoil.2010.10.003

    Article  Google Scholar 

  • Chimwamurombe PM, Grönemeyer JL, Reinhold-Hurek B (2016) Isolation and characterization of culturable seed-associated bacterial endophytes from gnotobiotically grown Marama bean seedlings. FEMS Microbiol Ecol 92:fiw083. doi:10.1093/femsec/fiw083

    Article  PubMed  Google Scholar 

  • de Voogd NJ, Cleary DF, Polónia AR, Gomes NC (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, west java, Indonesia. FEMS Microbiol Ecol 91:fiv019. doi:10.1093/femsec/fiv019

    Article  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 72:5069–5072. doi:10.1128/AEM.03006-05

    Article  CAS  Google Scholar 

  • Dimitroula H, Syranidou E, Manousaki E, Nikolaidis NP, Karatzas GP, Kalogerakis N (2015) Mitigation measures for chromium-VI contaminated groundwater–the role of endophytic bacteria in rhizofiltration. J Hazard Mater 281:114–120. doi:10.1016/j.jhazmat.2014.08.005

    Article  CAS  PubMed  Google Scholar 

  • Dourado MN, Aparecida Camargo, NAS, Souza SD, Araújo WL (2015) Biotechnological and agronomic potential of endophytic pink-pigmented methylotrophic Methylobacterium spp. BioMed Research International 909016. doi: 10.1155/2015/909016

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  • Griffiths E, Gupta RS (2007) Identification of signature proteins that are distinctive of the Deinococcus-Thermus phylum. Int Microbiol 10:201–208

    CAS  PubMed  Google Scholar 

  • Guttman DS, McHardy AC, Schulze-Lefert P (2014) Microbial genome-enabled insights into plant-microorganism interactions. Nat Rev Genet 15:797–813

    Article  CAS  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

  • Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. doi:10.1016/j.tim.2008.07.008

    Article  CAS  PubMed  Google Scholar 

  • Hardoim PR, Hardoim CCP, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e340438. doi:10.1371/journal.pone.0030438

    Google Scholar 

  • Hong C, Si Y, Xing Y, Li Y (2015) Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ Sci Pollut R 22:10788–10799. doi:10.1007/s11356-015-4186-3

    Article  CAS  Google Scholar 

  • 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 70:2667–2677. doi:10.1128/AEM.70.5.2667-2677.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • INEGI (National Institute of Informatics, Geography and Statistics, Mexico) (2009) Prontuario de información geográfica municipal de los Estados Unidos Mexicanos. Zimapan, Hidalgo. Available in: www.inegi.org.mx

  • Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72. doi:10.2478/intox-2014-0009

    Article  PubMed  PubMed Central  Google Scholar 

  • Joe MM, Devaraj S, Benson A, Sa T (2016) Isolation of phosphate solubilizing endophytic bacteria from Phyllanthus amarus Schum & Thonn: evaluation of plant growth promotion and antioxidant activity under salt stress. Journal of Applied Research on Medicinal and Aromatic Plants 3:71–77. doi:10.1016/j.jarmap.2016.02.003

    Article  Google Scholar 

  • Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396. doi:10.1371/journal.pone.0020396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston-Monje D, Lundberg DS, Lazarovits G, Reis VM, Raizada MN (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil. doi:10.1007/s11104-016-2826-01-19

    Google Scholar 

  • Khan MU, Sessitsch A, Harris M, Fatima K, Imran A, Arslan M et al (2015) Cr-resistant rhizo-and endophytic bacteria associated with Prosopis juliflora and their potential as phytoremediation enhancing agents in metal-degraded soils. Front Plant Sci 5:10–3389. doi:10.3389/fpls.2014.00755

    Article  Google Scholar 

  • Kidd P, Mench M, Alvarez-Lopez V, Bert V, Dimitriou I, Friesl-Hanl W et al (2015) Agronomic practices for improving gentle remediation of trace element-contaminated soils. Int J Phytoremediat 17:1005–1037. doi:10.1080/15226514.2014.1003788

    Article  CAS  Google Scholar 

  • Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. doi:10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YM, Kim EH, Lee HK, Hong SG (2014) Biodiversity and physiological characteristics of Antarctic and Arctic lichens-associated bacteria. World J Microb Biot 30:2711–2721. doi:10.1007/s11274-014-1695-z

    Article  CAS  Google Scholar 

  • Lopez-Velasco G, Carder PA, Welbaum GE, Ponder MA (2013) Diversity of the spinach (Spinacia oleracea) spermosphere and phyllosphere bacterial communities. FEMS Microbiol Lett 346:146–154. doi:10.1111/1574-6968.12216

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonelli C et al (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce Cd phytotoxicity. Int J Phytoremediat 11:252–267. doi:10.1080/15226510802432678

    Article  Google Scholar 

  • Mench M, Lepp N, Bert V, Schwitzguébel JP, Gawronski SW, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST action 859. J Soils Sediments 10:1039–1070. doi:10.1007/s11368-010-0190-x

    Article  CAS  Google Scholar 

  • Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, Van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mesa J, Mateos-Naranjo E, Caviedes MA, Redondo-Gómez S, Pajuelo E, Rodríguez-Llorente ID (2015) Endophytic cultivable bacteria of the metal bioaccumulator Spartina maritima improve plant growth but not metal uptake in polluted marshes soils. Front Microbiol 6. doi:10.3389/fmicb.2015.01450

  • Pereira LB, Vicentini R, Ottoboni LM (2015) Characterization of the core microbiota of the drainage and surrounding soil of a Brazilian copper mine. Genet Mol Biol 38:484–489. doi:10.1590/S1415-475738420150025

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin S, Miao Q, Feng WW, Wang Y, Zhu X, Xing K, Jiang JH (2015) Biodiversity and plant growth promoting traits of culturable endophytic actinobacteria associated with Jatropha curcas L. growing in Panxi dry-hot valley soil. Appl Soil Ecol 93:47–55. doi:10.1016/j.apsoil.2015.04.004

    Article  Google Scholar 

  • Quince C, Lanzén A, Curtis TP, Davenport RJ, Hall N, Head IM, Read LF, Sloan WT (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:639–641

    Article  CAS  PubMed  Google Scholar 

  • Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160. doi:10.1016/j.chemosphere.2009.06.047

    Article  CAS  PubMed  Google Scholar 

  • Román-Ponce B, Li YH, Vásquez-Murrieta MS, Sui XH, Chen WF, Estrada-De Los Santos P, Wang ET (2015) Brevibacterium metallicus sp. nov., an endophytic bacterium isolated from roots of Prosopis laegivata grown at the edge of a mine tailing in Mexico. Arch Microbiol 197:1151–1158. doi:10.1007/s00203-015-1156-6

    Article  PubMed  Google Scholar 

  • Rzedowsky J, Rzedowsky GC (1985) Flora Fanerogámica del Valle de México Volume II Dicotyledoneae. Escuela Nacional de Ciencias Biológicas e Instituto de Ecología, Mexico City

    Google Scholar 

  • Sánchez-López AS (2015) Basis for the remediation of sites polluted by potentially toxic elements in Zimapan, Hgo., Mexico: interdisciplinary approach. Ph D Thesis. Hasselt University – Colegio de Postgraduados

  • Sánchez-López AS, González-Chávez MDCA, Carrillo-González R, Vangronsveld J, Díaz-Garduño M (2015) Wild flora of mine tailings: perspectives for use in phytoremediation of potentially toxic elements in a semi-arid region in Mexico. Int J Phytoremediat 17:476–484. doi:10.1080/15226514.2014.922922

    Article  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. doi:10.1186/gb-2011-12-6-r60.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun L, Qiu F, Zhang X, Dai X, Dong X, Song W (2008) Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microbial Ecol 55:415–424. doi:10.1007/s00248-007-9287-1

    Article  CAS  Google Scholar 

  • Sy A, Timmers ACJ, Knief C, Vorholt JA (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71:7245–7252. doi:10.1128/AEM.71.11.7245-7252.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Truyens S, Weyens N, Cuypers A, Vangronsveld J (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol 15:971–981. doi:10.1111/j.1438-8677.2012.00711.x

    Article  CAS  PubMed  Google Scholar 

  • Truyens S, Jambon I, Croes S, Janssen J, Weyens N, Mench M et al (2014) The effect of long-term Cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int J Phytoremediat 16:643–659. doi:10.1080/15226514.2013.837027

    Article  CAS  Google Scholar 

  • Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50. doi:10.1111/1758-2229.12181

    Article  Google Scholar 

  • Truyens S, Beckers B, Thijs S, Weyens N, Cuypers A, Vangronsveld J (2016) Cadmium-induced and trans-generational changes in the cultivable and total seed endophytic community of Arabidopsis thaliana. Plant Biol 18:376–381. doi:10.1111/plb.12415

    Article  CAS  PubMed  Google Scholar 

  • Udeigwe TK, Teboh JM, Eze PN, Hashem Stietiya M, Kumar V, Hendrix J, Mascagni HJ Jr, Ying T, Kandakji T (2015) Implications of leading crop production practices on environmental quality and human health. J Environ Manag 151:267–279. doi:10.1016/j.jenvman.2014.11.024

    Article  CAS  Google Scholar 

  • Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206. doi:10.1111/nph.13312

    Article  PubMed  Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Theys T, Vassilev A, Meers E, Nehnevajova E (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794. doi:10.1007/s11356-009-0213-6

    Article  CAS  Google Scholar 

  • Visioli G, D’Egidio S, Vamerali T, Mattarozzi M, Sanangelantoni AM (2014) Culturable endophytic bacteria enhance Ni translocation in the hyperaccumulator Noccaea caerulescens. Chemosphere 117:538–544. doi:10.1016/j.chemosphere.2014.09.014

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xu L, Shen H, Wang J, Liu W, Zhu X et al (2015) Metabolomic analysis with GC-MS to reveal potential metabolites and biological pathways involved in Pb & Cd stress response of radish roots. Sci Rep 5:18296. doi:10.1038/srep18296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wani ZA, Ashraf N, Mohiuddin T, Hassan SRU (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965. doi:10.1007/s00253-015-6487-3

    Article  CAS  PubMed  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotech 20:248–254. doi:10.1016/j.copbio.2009.02.012

    Article  CAS  PubMed  Google Scholar 

  • Weyens N, Gielen M, Beckers B, Boulet J, Lelie D, Taghavi S et al (2014) Bacteria associated with yellow lupine grown on a metal-contaminated soil: in vitro screening and in vivo evaluation for their potential to enhance Cd phytoextraction. Plant Biol 16:988–996. doi:10.1111/plb.12141

    Article  CAS  PubMed  Google Scholar 

  • Xiao E, Krumins V, Dong Y, Xiao T, Ning Z, Xiao Q, Sun W (2016) Microbial diversity and community structure in an antimony-rich tailings dump. Appl Microbiol Biot 1–13. doi: 10.1007/s00253-016-7598-1

  • Xu XH, Wang C, Li SX, Su ZZ, Zhou HN, Mao LJ et al (2015) Friend or foe: differential responses of rice to invasion by mutualistic or pathogenic fungi revealed by RNAseq and metabolite profiling. Scientific Reports 5:13624. doi:10.1038/srep13624

    Article  PubMed  PubMed Central  Google Scholar 

  • Yadav AN, Sachan SG, Verma P, Saxena AK (2015) Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. J Biosci Bioeng 119:683–693. doi:10.1016/j.jbiosc.2014.11.006

    Article  CAS  PubMed  Google Scholar 

  • Zhang YF, He LY, Chen ZJ, Zhang WH, Wang QY, Qian M, Sheng XF (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725. doi:10.1016/j.jhazmat.2010.12.069

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported by a BOF-BILA grant from Hasselt University, the Hasselt University Methusalem project 08M03VGRJ and was also part of the CONACYT project PDCPN2013-1-215241.

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Correspondence to Jaco Vangronsveld.

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Sánchez-López, A.S., Thijs, S., Beckers, B. et al. 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 (2018). https://doi.org/10.1007/s11104-017-3176-2

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