Environmental Science and Pollution Research

, Volume 23, Issue 10, pp 10200–10214 | Cite as

Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: phylogenetic diversity, functional characterization, and influence of metal(loid) contamination

  • Cátia Fidalgo
  • Isabel Henriques
  • Jaqueline Rocha
  • Marta Tacão
  • Artur Alves
Research Article

Abstract

Halimione portulacoides is abundant in salt marshes, accumulates mercury (Hg), and was proposed as useful for phytoremediation and pollution biomonitoring. Endophytic bacteria promote plant growth and provide compounds with industrial applications. Nevertheless, information about endophytic bacteria from H. portulacoides is scarce. Endophytic isolates (n = 665) were obtained from aboveground and belowground plant tissues, from two Hg-contaminated sites (sites E and B) and a noncontaminated site (site C), in the estuary Ria de Aveiro. Representative isolates (n = 467) were identified by 16S rRNA gene sequencing and subjected to functional assays. Isolates affiliated with Proteobacteria (64 %), Actinobacteria (23 %), Firmicutes (10 %), and Bacteroidetes (3 %). Altererythrobacter (7.4 %), Marinilactibacillus (6.4 %), Microbacterium (10.2 %), Salinicola (8.8 %), and Vibrio (7.8 %) were the most abundant genera. Notably, Salinicola (n = 58) were only isolated from site C; Hoeflea (17), Labrenzia (22), and Microbacterium (67) only from belowground tissues. This is the first report of Marinilactibacillus in the endosphere. Principal coordinate analysis showed that community composition changes with the contamination gradient and tissue. Our results suggest that the endosphere of H. portulacoides represents a diverse bacterial hotspot including putative novel species. Many isolates, particularly those affiliated to Altererythrobacter, Marinilactibacillus, Microbacterium, and Vibrio, tested positive for enzymatic activities and plant growth promoters, exposing H. portulacoides as a source of bacteria and compounds with biotechnological applications.

Keywords

Endophyte Bacteria Halimione portulacoides Salt marsh plants Plant growth promotion Extracellular enzymes 

Notes

Acknowledgments

This work was financed by the European Funds through COMPETE and by National Funds through the Portuguese Foundation for Science and Technology (FCT) within project PhytoMarsh (PTDC/AAC-AMB/118873/2010–FCOMP-01-0124-FEDER-019328). The authors acknowledge FCT financing to CESAM (UID/AMB/50017/2013) and Institute for Research in Biomedicine (iBiMED–UID/BIM/04501/2013), Artur Alves (FCT Investigator Programme–IF/00835/2013), Isabel Henriques (FCT Investigator Programme–IF/00492/2013), and Cátia Fidalgo (PhD grant–SFRH/BD/85423/2012).

Authors acknowledge Paula Castro and Diogo Proença for kindly providing positive and negative control strains used in this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2016_6208_MOESM1_ESM.pdf (455 kb)
ESM 1(PDF 454 kb)
11356_2016_6208_MOESM2_ESM.pdf (418 kb)
ESM 2(PDF 417 kb)
11356_2016_6208_MOESM3_ESM.pdf (422 kb)
ESM 3(PDF 422 kb)
11356_2016_6208_MOESM4_ESM.pdf (842 kb)
ESM 4(PDF 841 kb)

References

  1. Aafi NE, Saidi N, Maltouf AF, Perez-Palacios P, Dary M, Brhada F, Pajuelo E (2015) Prospecting metal-tolerant rhizobia for phytoremediation of mining soils from Morocco using Anthyllis vulneraria L. Environ Sci Pollut Res 22:4500–4512. doi:10.1007/s11356-014-3596-y CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389 CrossRefGoogle Scholar
  3. Alongi DM (1998) Mangroves and salt marshes. In: Kennish MJ, Lutz PL (eds) Coastal ecosystem processes. CRC, Florida, 419 pp. ISBN 0-8493-8426-5Google Scholar
  4. Alves A, Correia A, Igual JM, Trujillo ME (2014) Microbacterium endophyticum sp. nov. and Microbacterium halimionae sp. nov., endophytes isolated from the salt-marsh plant Halimione portulacoides and emended description of the genus Microbacterium. Syst Appl Microbiol 37:474–479. doi:10.1016/j.syapm.2014.08.004 CrossRefGoogle Scholar
  5. Alves A, Riesco R, Correia A, Trujillo ME (2015) Microbacterium proteolyticum sp. nov. isolated from roots of Halimione portulacoides. Int J Syst Evol Microbiol 65:1794–1798. doi:10.1099/ijs.0.000177 CrossRefGoogle Scholar
  6. Ando S, Goto M, Meunchang S, Thongra-ar P, Fujiwara T, Hayashi H, Yoneyama T (2005) Detection of nifH sequences in sugarcane (Saccharum officinarum L.) and pineapple (Ananas comosus [L.] Merr.). Soil Sci Plant Nutr 51:303–308. doi:10.1111/j.1747-0765.2005.tb00034.x CrossRefGoogle Scholar
  7. Anjum NA, Ahmad I, Válega M, Pacheco M, Figueira E, Duarte AC, Pereira E (2011) Impact of seasonal fluctuations on the sediment-mercury, its accumulation and partitioning in Halimione portulacoides and Juncus maritimus collected from Ria de Aveiro coastal lagoon (Portugal). Water Air Soil Pollut 222:1–15. doi:10.1007/s11270-011-0799-4 CrossRefGoogle Scholar
  8. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148. doi:10.3389/fmicb.2014.00148 Google Scholar
  9. Bibi F, Jeong JH, Chung EJ, Jeon CO, Chung YR (2014) Labrenzia suaedae sp. nov., a marine bacterium isolated from a halophyte, and emended description of the genus Labrenzia. Int J Syst Evol Microbiol 64:1116–1122. doi:10.1099/ijs.0.052860-0 CrossRefGoogle Scholar
  10. Bouchard V, Creach V, Lefeuvre JC, Bertru G, Mariotti A (1998) Fate of plant detritus in a European salt marsh dominated by Atriplex portulacoides (L.) Aellen. Hydrobiologia 373:75–87CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. Carvalho PN, Basto MCP, Silva MFGM, Machado A, Bordalo AA, Vasconcelos TSD (2010) Ability of salt marsh plants for TBT remediation in sediments. Environ Sci Pollut Res 17:1279–1286. doi:10.1007/s11356-010-0307-1 CrossRefGoogle Scholar
  13. Costa C, Jesus-Rydin C (2001) Site investigation on heavy metals contaminated ground in Estarreja – Portugal. Eng Geol 60:39–47. doi:10.1016/S0013-7952(00)00087-9 CrossRefGoogle Scholar
  14. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 41:D633–D642. doi:10.1093/nar/gkt1244 CrossRefGoogle Scholar
  15. Couto MNPFS, Basto MCP, Vasconcelos MTSD (2011) Suitability of different salt marsh plants for petroleum hydrocarbons remediation. Chemosphere 84:1052–1057. doi:10.1016/j.chemosphere.2011.04.069 CrossRefGoogle Scholar
  16. Cox CD (1994) Deferration of laboratory media and assays for ferric and ferrous ions. Method Enzymol 235:315–329. doi:10.1016/0076-6879(94)35150-3 CrossRefGoogle Scholar
  17. De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574. doi:10.1890/08-1823.1 CrossRefGoogle Scholar
  18. Dworkin M, Foster JW (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–603Google Scholar
  19. Ellis RJ, Neish B, Trett MW, Best JG, Weightman AJ, Morgan P, Fry JC (2001) Comparison of microbial and meiofaunal community analyses for determining impact of heavy metal contamination. J Microbiol Meth 45:171–185. doi:10.1016/S0167-7012(01)00245-7 CrossRefGoogle Scholar
  20. Ellis RJ, Morgan P, Weightman AJ, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl Environ Microb 69:3223–3230. doi:10.1128/AEM.69.6.3223-3230.2003 CrossRefGoogle Scholar
  21. Figueira E, Freitas R (2013) Consumption of Ruditapes philippinarum and Ruditapes decussatus: comparison of element accumulation and health risk. Environ Sci Pollut R 20:5682–5691. doi:10.1007/s11356-013-1587-z CrossRefGoogle Scholar
  22. Gaby JC, Buckley DH (2012) A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE 7:7. doi:10.1371/journal.pone.0042149 CrossRefGoogle Scholar
  23. Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. Jafari SA, Cheraghi S, Mirbakhsh M, Mirza R, Maryamabadi A (2015) Employing response surface methodology for optimization of mercury bioremediation by Vibrio parahaemolyticus PG02 in Coastal Sediments of Bushehr, Iran. CLEAN 43:118–126. doi:10.1002/clen.201300616 Google Scholar
  26. Jose PA, Sundari IS, Sivakala KK, Jebahumar SRD (2014) Molecular phylogeny and plant growth promoting traits of endophytic bacteria isolated from roots of seagrass Cymodocea serrulata. Indian J Geo-Mar Sci 43:571–579Google Scholar
  27. Karnwal A (2009) Production of indole acetic acid by fluorescent Pseudomonas in the presence of L-tryptophan and rice root exudates. J of Plant Pathol 91:61–63Google Scholar
  28. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Micr 62:716–721. doi:10.1099/ijs.0.038075-0 CrossRefGoogle Scholar
  29. Kim Y-J, Nguyen N-L, Hoang V-A, Min J-W, Hwang K-H, Yang D-C (2015) Microbacterium panaciterrae sp. nov., isolated from the rhizosphere of ginseng. Int J Syst Evol Micr 65:927–933. doi:10.1099/ijs.0.000041 CrossRefGoogle Scholar
  30. Kiyohara M, Sakaguchi K, Yamaguchi K, Akari T, Nakamura T, Ito M (2005) Molecular cloning and characterization of a novelβ-1,3-xylanase possessing two putative carbohydrate-binding modules from a marine bacterium Vibrio sp. strain AX-4. Biochem J 388:949–957. doi:10.1042/BJ20050190 CrossRefGoogle Scholar
  31. Kukla M, Płociniczak T, Piotrowska-Seget Z (2014) Diversity of endophytic bacteria in Lolium perenne and their potential to degrade petroleum hydrocarbons and promote plant growth. Chemosphere 117:40–46. doi:10.1016/j.chemosphere.2014.05.055 CrossRefGoogle Scholar
  32. Kumar NR, Nair S (2007) Vibrio rhizosphaerae sp. nov., a red-pigmented bacterium that antagonizes phytopathogenic bacteria. Int J Syst Evol Micr 57:2241–2246. doi:10.1099/ijs.0.65017-0 CrossRefGoogle Scholar
  33. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, pp 115–175Google Scholar
  34. Liu XL, Liu SL, Liu M, Kong BH, Liu L, Li YH (2014) A primary assessment of the endophytic bacterial community in a xerophilous moss (Grimmia montana) using molecular method and cultivated isolates. Braz J Microbiol 45:163–173CrossRefGoogle Scholar
  35. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, van der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606. doi:10.1080/0735-260291044377 CrossRefGoogle Scholar
  36. Lozano-Rodriguez E, Hernández LE, Bonay P, Carpena-Ruiz RO (1997) Distribution of cadmium in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48:123–128CrossRefGoogle Scholar
  37. Lucena-Padrós H, Jiménez E, Maldonado-Barragán A, Rodríguez JM, Ruiz-Barba JL (2015) PCR-DGGE assessment of the bacterial diversity in Spanish-style green table-olive fermentations. Int J Food Microbiol 205:47–53. doi:10.1016/j.ijfoodmicro.2015.03.033 CrossRefGoogle Scholar
  38. Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manage 156:62–69. doi:10.1016/j.jenvman.2015.03.024 CrossRefGoogle Scholar
  39. Mora-Ruiz MR, Font-Verdera F, Díaz-Gil C, Urdiain M, Rodríguez-Valdecantos G, González B, Orfila A, Rosselló-Móra R (2015) Moderate halophilic bacteria colonizing the phylloplane of halophytes of the subfamily Salicornioideae (Amaranthaceae). Syst Appl Microbiol 38:406–416. doi:10.1016/j.syapm.2015.05.004 CrossRefGoogle Scholar
  40. Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. doi:10.1111/j.1574-6968.1999.tb13383.x CrossRefGoogle Scholar
  41. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: Community Ecology Package. R package version 2.2-1. http://CRAN.R-project.org/package=vegan
  42. Oliveira V, Gomes NCM, Almeida A, Silva AMS, Simões MQM, Smalla K, Cunha A (2014a) Hydrocarbon contamination and plant species determine the phylogenetic and functional diversity of endophytic degrading bacteria. Mol Ecol 23:1392–1404. doi:10.1111/mec.12559 CrossRefGoogle Scholar
  43. Oliveira V, Gomes NCM, Cleary DFR, Almeida A, Silva AMS, Simões MMQ, Silva H, Cunha A (2014b) Halophyte plant colonization as a driver of the composition of bacterial communities in salt marshes chronically exposed to oil hydrocarbons. FEMS Microbiol Ecol 90:647–662. doi:10.1111/1574-6941.12425 CrossRefGoogle Scholar
  44. Park HY, Kim KK, Jin L, Lee S-T (2006) Microbacterium paludicola sp. nov., a novel xylanolytic bacterium isolated from swamp forest. Int J Syst Evol Micr 56:535–539. doi:10.1099/ijs.0.63945-0 CrossRefGoogle Scholar
  45. Passari AK, Mishra VK, Saikia R, Gupta VK, Singh BP (2015) Isolation, abundance and phylogenetic affiliation of endophytic actinomycetes associated with medicinal plants and screening for their in vitro antimicrobial biosynthetic potential. Front Microbiol 6:273. doi:10.3389/fmicb.2015.00273 CrossRefGoogle Scholar
  46. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plantarum 118:10–15. doi:10.1034/j.1399-3054.2003.00086.x CrossRefGoogle Scholar
  47. Pereira ME, Duarte AC, Millward GE, Vale C, Abreu SN (1998) Tidal export of particulate mercury from the most contaminated area of Aveiro’s Lagoon, Portugal. Sci Total Environ 213:157–163. doi:10.1016/S0048-9697(98)00087-4 CrossRefGoogle Scholar
  48. Pereira ME, Lillebø AI, Pato P, Válega M, Coelho JP, Lopes CB, Rodrigues S, Chachada A, Otero M, Pardal MA, Duarte AC (2009) Mercury pollution in Ria de Aveiro (Portugal): a review of the system assessment. Environ Monit Assess 155:39–49. doi:10.1007/s10661-008-0416-1 CrossRefGoogle Scholar
  49. Pereira SIA, Barbosa L, Castro PML (2013) Rhizobacteria isolated from a metal-polluted area enhance plant growth in zinc and cadmium-contaminated soil. Int J Environ Sci Technol 12:2127–2142. doi:10.1007/s13762-014-0614-z CrossRefGoogle Scholar
  50. Pérez‐Miranda S, Cabirol N, George‐Téllez R, Zamudio‐Rivera LS, Fernández FJ (2007) O‐CAS, a fast and universal method for siderophore detection. J Microbiol Meth 70:127–131. doi:10.1016/j.mimet.2007.03.023 CrossRefGoogle Scholar
  51. Pohlert T (2005) PMCMR: Calculate Pairwise Multiple Comparisons of Mean Rank Sums. R package version 1.1. http://CRAN.R-project.org/package=PMCMR
  52. Proença DN, Francisco R, Santos CV, Lopes A, Fonseca L, Abrantes IMO, Morais PV (2010) Diversity of bacteria associated with Bursaphelenchus xylophilus and other nematodes isolated from Pinus pinaster trees with pine wilt disease. PLoS One 5:12. doi:10.1371/journal.pone.0015191 CrossRefGoogle Scholar
  53. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
  54. Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574. doi:10.1016/j.biotechadv.2012.04.011 CrossRefGoogle Scholar
  55. Rameshkumar N, Krishnan R, Lang E, Matsumura Y, Sawabe T, Sawabe T (2014) Zunongwangia mangrovi sp. nov., isolated from mangrove (Avicennia marina) rhizosphere, and emended description of the genus Zunongwangia. Int J Syst Evol Microbiol 64:545–550. doi:10.1099/ijs.0.053512-0 CrossRefGoogle Scholar
  56. Ray AK, Ghosh K, Ringø E (2012) Enzyme-producing bacteria isolated from fish gut: a review. Aquacult Nutr 18:465–492. doi:10.1111/j.1365-2095.2012.00943.x CrossRefGoogle Scholar
  57. Romanenko LA, Tanaka N, Kalinovskaya NI, Mikhailov VV (2013) Antimicrobial potential of deep surface sediment associated bacteria from the Sea of Japan. World J Microb Biot 29:1169–1177. doi:10.1007/s11274-013-1276-6 CrossRefGoogle Scholar
  58. Roth E, Schwenninger SM, Hasler M, Eugster-Meier E, Lacroix C (2010) Population dynamics of two antilisterial cheese surface consortia revealed by temporal temperature gradient gel electrophoresis. BMC Microbiol 10:74. doi:10.1186/1471-2180-10-74 CrossRefGoogle Scholar
  59. Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194. doi:10.1016/j.soilbio.2013.01.012 CrossRefGoogle Scholar
  60. Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170. doi:10.1016/j.envpol.2008.04.007 CrossRefGoogle Scholar
  61. Tanaka T, Kawasaki K, Daimon S, Kitagawa W, Yamamoto K, Tamaki H, Tanaka M, Nakatsu CH, Kamagata Y (2014) A hidden pitfall in agar media preparation undermines cultivability of microorganisms. Appl Environ Microbiol 80:7659–7666. doi:10.1128/AEM.02741-14 CrossRefGoogle Scholar
  62. Thompson FL, Iida T, Swings J (2004) Biodiversity of Vibrios. Microbiol Mol Biol R 68:403–431. doi:10.1128/MMBR.68.3.403-431.2004 CrossRefGoogle Scholar
  63. Toffin L, Zink K, Kato C, Pignet P, Bidault A, Bienvenu N, Birrien J-L, Prieur D (2005) Marinilactibacillus piezotolerans sp. nov., a novel marine lactic acid bacterium isolated from deep sub-seafloor sediment of the Nankai Trough. Int J Syst Evol Microbiol 55:345–351. doi:10.1099/ijs.0.63236-0 CrossRefGoogle Scholar
  64. Válega M, Lillebø AI, Pereira ME, Caçador I, Duarte AC, Pardal MA (2008a) Mercury in salt marshes ecosystems: Halimione portulacoides as biomonitor. Chemosphere 73:1224–1229. doi:10.1016/j.chemosphere.2008.07.053 CrossRefGoogle Scholar
  65. Válega M, Lillebø AI, Pereira ME, Duarte AC, Pardal MA (2008b) Long-term effects of Mercury in a salt marsh: hysteresis in the distribution of vegetation following recovery from contamination. Chemosphere 71:765–772. doi:10.1016/j.chemosphere.2007.10.013 CrossRefGoogle Scholar
  66. Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831CrossRefGoogle Scholar
  67. Versalovic J, Schneider M, de Brujin FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Method Mol Cell Biol 5:25–40Google Scholar
  68. Vinod V, Kumar A, Zachariah TJ (2014) Isolation, characterization and identification of pericarp-degrading bacteria for the production of off-odour-free white pepper from fresh berries of Piper nigrum L. J Appl Microbiol 116:890–902. doi:10.1111/jam.12431 CrossRefGoogle Scholar
  69. Woerner LS, Hackney CT (1997) Distribution of Juncus roemerianus in North Carolina tidal marshes: the importance of physical and biotic variables. Wetlands 17:284–291CrossRefGoogle Scholar
  70. Wu YH, Xu L, Meng FX, Zhang DS, Wang CS, Oren A, Xu X-W (2014) Altererythrobacter atlanticus sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 64:116–121. doi:10.1099/ijs.0.052951-0 CrossRefGoogle Scholar
  71. Zakhia F, Jeder H, Willems A, Gillis M, Dreyfus B, de Lajudie P (2006) Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microbial Ecol 51:375–393. doi:10.1007/s00248-006-9025-0 CrossRefGoogle Scholar
  72. Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microb 68:2198–2208. doi:10.1128/AEM.68.5.2198-2208.2002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Cátia Fidalgo
    • 1
    • 2
  • Isabel Henriques
    • 2
  • Jaqueline Rocha
    • 1
  • Marta Tacão
    • 1
  • Artur Alves
    • 1
  1. 1.CESAM, Departamento de BiologiaUniversidade de AveiroAveiroPortugal
  2. 2.iBiMED and CESAM, Departamento de BiologiaCampus de Santiago, Universidade de AveiroAveiroPortugal

Personalised recommendations