Skip to main content

Advertisement

Springer Nature Link
Log in

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

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Alongi DM (1998) Mangroves and salt marshes. In: Kennish MJ, Lutz PL (eds) Coastal ecosystem processes. CRC, Florida, 419 pp. ISBN 0-8493-8426-5

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • 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 373:75–87

    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  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dworkin M, Foster JW (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–603

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 43:571–579

    Google Scholar 

  • 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 91:61–63

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 115–175

    Google Scholar 

  • 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 45:163–173

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 48:123–128

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pohlert T (2005) PMCMR: Calculate Pairwise Multiple Comparisons of Mean Rank Sums. R package version 1.1. http://CRAN.R-project.org/package=PMCMR

  • 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

    Article  Google Scholar 

  • 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/

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831

    Article  CAS  Google Scholar 

  • 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 5:25–40

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Woerner LS, Hackney CT (1997) Distribution of Juncus roemerianus in North Carolina tidal marshes: the importance of physical and biotic variables. Wetlands 17:284–291

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. CESAM, Departamento de Biologia, Universidade de Aveiro, Aveiro, Portugal

    Cátia Fidalgo, Jaqueline Rocha, Marta Tacão & Artur Alves

  2. iBiMED and CESAM, Departamento de Biologia, Campus de Santiago, Universidade de Aveiro, 3810-193, Aveiro, Portugal

    Cátia Fidalgo & Isabel Henriques

Authors
  1. Cátia Fidalgo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabel Henriques
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaqueline Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marta Tacão
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Artur Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabel Henriques.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Robert Duran

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 454 kb)

ESM 2

(PDF 417 kb)

ESM 3

(PDF 422 kb)

ESM 4

(PDF 841 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fidalgo, C., Henriques, I., Rocha, J. et al. Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: phylogenetic diversity, functional characterization, and influence of metal(loid) contamination. Environ Sci Pollut Res 23, 10200–10214 (2016). https://doi.org/10.1007/s11356-016-6208-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-6208-1

Keywords

Search

Navigation