HOME  »  Members  »  Collaborators  »  PhD Students/Fellows
title Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: phylogenetic diversity, functional characterization, and influence of metal(loid) contamination
authors Fidalgo, C; Henriques, I; Rocha, J; Tacao, M; Alves, A
author full name Fidalgo, Catia; Henriques, Isabel; Rocha, Jaqueline; Tacao, Marta; Alves, Artur
title Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: phylogenetic diversity, functional characterization, and influence of metal(loid) contamination
nationality internacional
language English
document type Article
author keywords Endophyte; Bacteria; Halimione portulacoides; Salt marsh plants; Plant growth promotion; Extracellular enzymes
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.
author address [Fidalgo, Catia; Rocha, Jaqueline; Tacao, Marta; Alves, Artur] Univ Aveiro, Dept Biol, CESAM, P-3800 Aveiro, Portugal; [Fidalgo, Catia; Henriques, Isabel] Univ Aveiro, Dept Biol, iBiMED, Campus Santiago, P-3810193 Aveiro, Portugal; [Fidalgo, Catia; Henriques, Isabel] Univ Aveiro, Dept Biol, CESAM, Campus Santiago, P-3810193 Aveiro, Portugal
reprint address Henriques, I (reprint author), Univ Aveiro, Dept Biol, iBiMED, Campus Santiago, P-3810193 Aveiro, Portugal.; Henriques, I (reprint author), Univ Aveiro, Dept Biol, CESAM, Campus Santiago, P-3810193 Aveiro, Portugal.
e-mail address ihenriques@ua.pt
funding agency and grant number European Funds through COMPETE; National Funds through the Portuguese Foundation for Science and Technology (FCT) within project PhytoMarsh [PTDC/AAC-AMB/118873/2010-FCOMP-01-0124-FEDER-019328]; FCT [UID/AMB/50017/2013]; Institute for Research in Biomedicine [iBiMED-UID/BIM/04501/2013]; [IF/00835/2013]; [IF/00492/2013]; [SFRH/BD/85423/2012]
funding text 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 Catia Fidalgo (PhD grant-SFRH/BD/85423/2012).
cited references Aafi NE, 2015, ENVIRON SCI POLLUT R, V22, P4500, DOI [10.1007/s11356-014-3596-y, DOI 10.1007/S11356-014-3596-Y]; Alongi DM, 1998, COASTAL ECOSYSTEM PR; Alves A, 2014, SYST APPL MICROBIOL, V37, P474, DOI 10.1016/j.syapm.2014.08.004; Alves A, 2015, INT J SYST EVOL MICR, V65, P1794, DOI 10.1099/ijs.0.000177; Liu XL, 2014, BRAZ J MICROBIOL, V45, P163; Costa C, 2001, ENG GEOL, V60, P39, DOI 10.1016/S0013-7952(00)00087-9; Romanenko LA, 2013, WORLD J MICROB BIOT, V29, P1169, DOI 10.1007/s11274-013-1276-6; Nautiyal CS, 1999, FEMS MICROBIOL LETT, V170, P265, DOI 10.1111/j.1574-6968.1999.tb13383.x; Anjum NA, 2011, WATER AIR SOIL POLL, V222, P1, DOI 10.1007/s11270-011-0799-4; LozanoRodriguez E, 1997, J EXP BOT, V48, P123, DOI 10.1093/jxb/48.1.123; Kim OS, 2012, INT J SYST EVOL MICR, V62, P716, DOI 10.1099/ijs.0.038075-0; Valega M, 2008, CHEMOSPHERE, V73, P1224, DOI 10.1016/j.chemosphere.2008.07.053; Ma Y, 2015, J ENVIRON MANAGE, V156, P62, DOI 10.1016/j.jenvman.2015.03.024; Pereira ME, 2009, ENVIRON MONIT ASSESS, V155, P39, DOI 10.1007/s10661-008-0416-1; VERSALOVIC J, 1991, NUCLEIC ACIDS RES, V19, P6823, DOI 10.1093/nar/19.24.6823; Ray AK, 2012, AQUACULT NUTR, V18, P465, DOI 10.1111/j.1365-2095.2012.00943.x; Jose PA, 2014, INDIAN J GEO-MAR SCI, V43, P571; Toffin L, 2005, INT J SYST EVOL MICR, V55, P345, DOI 10.1099/ijs.0.63236-0; Sheng XF, 2008, ENVIRON POLLUT, V156, P1164, DOI 10.1016/j.envpol.2008.04.007; Kiyohara M, 2005, BIOCHEM J, V388, P949, DOI 10.1042/BJ20050190; Altschul SF, 1997, NUCLEIC ACIDS RES, V25, P3389, DOI 10.1093/nar/25.17.3389; DWORKIN M, 1958, J BACTERIOL, V75, P592; Lucena-Padros H, 2015, INT J FOOD MICROBIOL, V205, P47, DOI 10.1016/j.ijfoodmicro.2015.03.033; Rajkumar M, 2012, BIOTECHNOL ADV, V30, P1562, DOI 10.1016/j.biotechadv.2012.04.011; De Caceres M, 2009, ECOLOGY, V90, P3566; Bibi F, 2014, INT J SYST EVOL MICR, V64, P1116, DOI 10.1099/ijs.0.052860-0; Oliveira V, 2014, MOL ECOL, V23, P1392, DOI 10.1111/mec.12559; Carvalho PN, 2010, ENVIRON SCI POLLUT R, V17, P1279, DOI 10.1007/s11356-010-0307-1; GORDON SA, 1951, PLANT PHYSIOL, V26, P192, DOI 10.1104/pp.26.1.192; Rameshkumar N, 2014, INT J SYST EVOL MICR, V64, P545, DOI 10.1099/ijs.0.053512-0; Bulgarelli D, 2013, ANNU REV PLANT BIOL, V64, P807, DOI 10.1146/annurev-arplant-050312-120106; Ellis RJ, 2003, APPL ENVIRON MICROB, V69, P3223, DOI 10.1128/AEM.69.6.3223-3230.2003; Kumar NR, 2007, INT J SYST EVOL MICR, V57, P2241, DOI 10.1099/ijs.0.65017-0; Ando S, 2005, SOIL SCI PLANT NUTR, V51, P303, DOI 10.1111/j.1747-0765.2005.tb00034.x; Tanaka T, 2014, APPL ENVIRON MICROB, V80, P7659, DOI 10.1128/AEM.02741-14; Woerner LS, 1997, WETLANDS, V17, P284; Kukla M, 2014, CHEMOSPHERE, V117, P40, DOI 10.1016/j.chemosphere.2014.05.055; Perez-Miranda S, 2007, J MICROBIOL METH, V70, P127, DOI 10.1016/j.mimet.2007.03.023; Lodewyckx C, 2002, CRIT REV PLANT SCI, V21, P583, DOI 10.1080/0735-260291044377; Cole JR, 2014, NUCLEIC ACIDS RES, V42, pD633, DOI 10.1093/nar/gkt1244; Pereira ME, 1998, SCI TOTAL ENVIRON, V213, P157, DOI 10.1016/S0048-9697(98)00087-4; Valega M, 2008, CHEMOSPHERE, V71, P765, DOI 10.1016/j.chemosphere.2007.10.013; Zinniel DK, 2002, APPL ENVIRON MICROB, V68, P2198, DOI 10.1128/AEM.68.5.2198-2208.2002; Couto MNPFS, 2011, CHEMOSPHERE, V84, P1052, DOI 10.1016/j.chemosphere.2011.04.069; Thompson FL, 2004, MICROBIOL MOL BIOL R, V68, P403, DOI 10.1128/MMBR.68.3.403-431.2004; Jafari SA, 2015, CLEAN-SOIL AIR WATER, V43, P118, DOI 10.1002/clen.201300616; Sessitsch A, 2013, SOIL BIOL BIOCHEM, V60, P182, DOI 10.1016/j.soilbio.2013.01.012; Ellis RJ, 2001, J MICROBIOL METH, V45, P171, DOI 10.1016/S0167-7012(01)00245-7; Vinod V, 2014, J APPL MICROBIOL, V116, P890, DOI 10.1111/jam.12431; Karnwal A, 2009, J PLANT PATHOL, V91, P61; Park HY, 2006, INT J SYST EVOL MICR, V56, P535, DOI 10.1099/ijs.0.63945-0; Mora-Ruiz MD, 2015, SYST APPL MICROBIOL, V38, P406, DOI 10.1016/j.syapm.2015.05.004; Figueira E, 2013, ENVIRON SCI POLLUT R, V20, P5682, DOI 10.1007/s11356-013-1587-z; Hardoim PR, 2008, TRENDS MICROBIOL, V16, P463, DOI 10.1016/j.tim.2008.07.008; Zakhia F, 2006, MICROB ECOL, V51, P375, DOI 10.1007/s00248-006-9025-0; Wu YH, 2014, INT J SYST EVOL MICR, V64, P116, DOI 10.1099/ijs.0.052951-0; Berg G, 2014, FRONT MICROBIOL, V5, DOI 10.3389/fmicb.2014.00148; Bouchard V., 1998, Hydrobiologia, V373-374, P75, DOI 10.1023/A:1017026430513; COX CD, 1994, METHOD ENZYMOL, V235, P315; Gaby JC, 2012, PLOS ONE, V7, DOI 10.1371/journal.pone.0042149; Kim Y-J, 2015, INT J SYST EVOL MICR, V65, P927, DOI [10.1099/ijs.0.000041, DOI 10.1099/IJS.0.000041]; Lane DJ, 1991, NUCL ACID TECHNIQUES, P115; Oksanen J., 2015, VEGAN COMMUNITY ECOL; Oliveira V, 2014, FEMS MICROBIOL ECOL, V90, P647, DOI 10.1111/1574-6941.12425; Passari AK, 2015, FRONT MICROBIOL, V6, DOI 10.3389/fmicb.2015.00273; Penrose DM, 2003, PHYSIOL PLANTARUM, V118, P10, DOI 10.1034/j.1399-3054.2003.00086.x; Pereira SIA, 2015, INT J ENVIRON SCI TE, V12, P2127, DOI 10.1007/s13762-014-0614-z; Pohlert T, 2005, PMCMR CALCULATE PAIR; Proenca DN, 2010, PLOS ONE, V5, DOI 10.1371/journal.pone.0015191; R Core Team, 2014, R LANG ENV STAT COMP; Roth E, 2010, BMC MICROBIOL, V10, DOI 10.1186/1471-2180-10-74; Versalovic James, 1994, Methods in Molecular and Cellular Biology, V5, P25
cited reference count 72
publisher city HEIDELBERG
issn 0944-1344
29-character source abbreviation ENVIRON SCI POLLUT R
iso source abbreviation Environ. Sci. Pollut. Res.
publication date MAY
year published 2016
volume 23
issue 10
beginning page 10200
ending page 10214
digital object identifier (doi) 10.1007/s11356-016-6208-1
page count 15
web of science category Environmental Sciences
subject category Environmental Sciences & Ecology
document delivery number DM5WN
unique article identifier WOS:000376421400090
link http://dx.doi.org/10.1007/s11356-016-6208-1