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Version 3.18
Publication Type J
Authors Wang, M; Li, EQ; Liu, C; Jousset, A; Salles, JF
Author Full Name Wang, Miao; Li, Erqin; Liu, Chen; Jousset, Alexandre; Salles, Joana F.
Title Functionality of Root-Associated Bacteria along a Salt Marsh Primary Succession
Language English
Document Type Article
Author Keywords functionality; plant-associated bacteria; plant selective force; soil type; salt marsh chronosequence
Abstract Plant-associated bacteria are known for their high functional trait diversity, from which many are likely to play a role in primary and secondary succession, facilitating plant establishment in suboptimal soils conditions. Here we used an undisturbed salt marsh chronosequence that represents over 100 years of soil development to assess how the functional traits of plant associated bacteria respond to soil type, plant species and plant compartment. We isolated and characterized 808 bacterial colonies from the rhizosphere soil and root endosphere of two salt marsh plants, Limonium vulgare and Artemisia maritima, along the chronosequence. From these, a set of 59 strains (with unique BOX-PCR patterns, 16S rRNA sequence and unique to one of the treatments) were further screened for their plant growth promoting traits (siderophore production, IAA production, exoprotease production and biofilm formation), traits associated with bacterial fitness (antibiotic and abiotic stress resistance - pH, osmotic and oxidative stress, and salinity) and metabolic potential. An overall view of functional diversity (multivariate analysis) indicated that the distributional pattern of bacterial functional traits was driven by soil type. Samples from the late succession (Stage 105 year) showed the most restricted distribution, harboring strains with relatively low functionalities, whereas the isolates from intermediate stage (35 year) showed a broad functional profiles. However, strains with high trait performance were largely from stage 65 year. Grouping the traits according to category revealed that the functionality of plant endophytes did not vary along the succession, thus being driven by plant rather than soil type. In opposition, the functionality of rhizosphere isolates responded strongly to variations in soil type as observed for antibiotic resistance (P = 0.014). Specifically, certain Pseudomonas sp. and Serratia sp. strains revealed high resistance against abiotic stress and antibiotics and produce more siderophores, confirming the high plant-growth promoting activity of these two genera. Overall, this study contributes to a better understanding of the functional diversity and adaptation of the microbiome at typical salt marsh plant species across soil types. Specifically, soil type was influential only in the rhizosphere but not on the endosphere, indicating a strong plant-driven effect on the functionality of endophytes.
Author Address [Wang, Miao; Salles, Joana F.] Univ Groningen, Groningen Inst Evolutionary Life Sci, Genom Res Ecol & Evolut Nat, Res Grp Microbial Community Ecol, Groningen, Netherlands; [Li, Erqin; Liu, Chen] Univ Utrecht, Dept Biol, Plant Microbe Interact, Utrecht, Netherlands; [Jousset, Alexandre] Univ Utrecht, Ecol & Biodivers, Utrecht, Netherlands
Reprint Address Wang, M (reprint author), Univ Groningen, Groningen Inst Evolutionary Life Sci, Genom Res Ecol & Evolut Nat, Res Grp Microbial Community Ecol, Groningen, Netherlands.
E-mail Address m.wang@rug.nl
ResearcherID Number Falcao Salles, Joana/A-7313-2008
Funding Agency and Grant Number China Scholarship Council
Funding Text We thank Han Olff, Matty Berg, Chris Smit, Maarten Schrama, and Ruth Howison for information on sampling locations and plant species. We are grateful to Jolanda K. Brons and Armando Cavalcante Franco Dias for sampling expeditions. We thank the 'Nederlandse Vereniging voor Natuurmonumenten' for granting us access to the salt marsh. This work was supported by China Scholarship Council, on a personal grant to MW.
Cited References Ahmed E, 2014, MICROB BIOTECHNOL, V7, P196, DOI 10.1111/1751-7915.12117; ALEXANDER DB, 1991, BIOL FERT SOILS, V12, P39, DOI 10.1007/BF00369386; BARNESS E, 1991, PLANT SOIL, V130, P231, DOI 10.1007/BF00011878; Bednarek P, 2010, CURR OPIN PLANT BIOL, V13, P378, DOI 10.1016/j.pbi.2010.05.002; Beneduzi A, 2012, GENET MOL BIOL, V35, P1044, DOI 10.1590/S1415-47572012000600020; Berendsen RL, 2012, TRENDS PLANT SCI, V17, P478, DOI 10.1016/j.tplants.2012.04.001; Berg G, 2006, FEMS MICROBIOL ECOL, V56, P250, DOI 10.1111/j.1574-6941.2005.00025.x; Berg G, 2002, APPL ENVIRON MICROB, V68, P3328, DOI 10.1128/AEM.68.7.3328-3338.2002; Berg G, 2014, FRONT MICROBIOL, V5, DOI 10.3389/fmicb.2014.00148; Berg G, 2009, FEMS MICROBIOL ECOL, V68, P1, DOI 10.1111/j.1574-6941.2009.00654.x; Bevivino A, 1998, FEMS MICROBIOL ECOL, V27, P225, DOI 10.1111/j.1574-6941.1998.tb00539.x; Bharathkumar S, 2008, J BASIC MICROB, V48, P10, DOI 10.1002/jobm.200700282; Brusetti L, 2008, BMC MICROBIOL, V8, DOI 10.1186/1471-2180-8-220; CAVALLISFORZA LL, 1967, AM J HUM GENET, V19, P233; Chin-A-Woeng TFC, 2003, NEW PHYTOL, V157, P503, DOI 10.1046/j.1469-8137.2003.00686.x; Cho JC, 2000, APPL ENVIRON MICROB, V66, P5448, DOI 10.1128/AEM.66.12.5448-5456.2000; Cibichakravarthy B, 2012, WORLD J MICROB BIOT, V28, P605, DOI 10.1007/s11274-011-0853-9; Compant S, 2005, APPL ENVIRON MICROB, V71, P1685, DOI 10.1128/AEM.71.4.1685-1693.2005; Compant S, 2010, SOIL BIOL BIOCHEM, V42, P669, DOI 10.1016/j.soilbio.2009.11.024; Costa R, 2006, FEMS MICROBIOL ECOL, V56, P236, DOI 10.1111/j.1574-6941.2006.00026.x; Crosa JH, 1997, MICROBIOL MOL BIOL R, V61, P319; Daane LL, 2001, APPL ENVIRON MICROB, V67, P2683, DOI 10.1128/AEM.67.6.2683-2691.2001; de Bello F, 2015, FOLIA GEOBOT, V50, P349, DOI 10.1007/s12224-015-9228-6; Dimkpa CO, 2009, SOIL BIOL BIOCHEM, V41, P154, DOI 10.1016/j.soilbio.2008.10.010; Dini-Andreote F, 2016, ISME J, V10, P1984, DOI 10.1038/ismej.2015.254; Dini-Andreote F, 2015, P NATL ACAD SCI USA, V112, pE1326, DOI 10.1073/pnas.1414261112; Dini-Andreote F, 2014, ISME J, V8, P1989, DOI 10.1038/ismej.2014.54; Dwivedi D, 2003, CURR SCI INDIA, V85, P1693; EDWARDS U, 1989, NUCLEIC ACIDS RES, V17, P7843, DOI 10.1093/nar/17.19.7843; Egamberdieva D, 2008, ENVIRON MICROBIOL, V10, P1, DOI 10.1111/j.1462-2920.2007.01424.x; Ellis RJ, 2003, APPL ENVIRON MICROB, V69, P3223, DOI 10.1128/AEM.69.6.3223-3230.2003; Faure D, 2009, PLANT SOIL, V321, P279, DOI 10.1007/s11104-008-9839-2; FELSENSTEIN J, 1981, J MOL EVOL, V17, P368, DOI 10.1007/BF01734359; Felsenstein J, 1993, PHYLOGENY INFERENCE; Gaiero JR, 2013, AM J BOT, V100, P1738, DOI 10.3732/ajb.1200572; Garbeva P, 2004, ANNU REV PHYTOPATHOL, V42, P243, DOI 10.1146/annurev.phyto.42.012604.135455; Garbeva P, 2004, FEMS MICROBIOL ECOL, V47, P51, DOI 10.1016/S0168-6496(03)00234-4; Gaujoux R., 2015, ALGORITHMS FRAMEWORK; Gayathri S, 2010, INDIAN J BIOTECHNOL, V9, P397; GLICKMANN E, 1995, APPL ENVIRON MICROB, V61, P793; GORDON SA, 1951, PLANT PHYSIOL, V26, P192, DOI 10.1104/pp.26.1.192; Grimont F, 2006, PROKARYOTES: A HANDBOOK ON THE BIOLOGY OF BACTERIA, VOL 6, THIRD EDITION, P219, DOI 10.1007/0-387-30746-x_11; Haas D, 2005, NAT REV MICROBIOL, V3, P307, DOI 10.1038/nrmicro1129; Haas D, 2003, ANNU REV PHYTOPATHOL, V41, P117, DOI 10.1146/annurev.phyto.41.052002.095656; Haichar FE, 2008, ISME J, V2, P1221, DOI 10.1038/ismej.2008.80; Hallmann J, 1997, CAN J MICROBIOL, V43, P895, DOI 10.1139/m97-131; Hardoim PR, 2008, TRENDS MICROBIOL, V16, P463, DOI 10.1016/j.tim.2008.07.008; Hartmann A, 2009, PLANT SOIL, V321, P235, DOI 10.1007/s11104-008-9814-y; Hong Y., 2013, CAN J MICROBIOL, V733, P1, DOI [10.1139/cjm-2015, DOI 10.1139/CJM-2015]; Hothorn T, 2008, BIOMETRICAL J, V50, P346, DOI 10.1002/bimj.200810425; Hussain Q, 2011, APPL SOIL ECOL, V48, P210, DOI 10.1016/j.apsoil.2011.03.004; Inceoglu O, 2010, APPL ENVIRON MICROB, V76, P3675, DOI 10.1128/AEM.00040-10; Jousset A, 2006, APPL ENVIRON MICROB, V72, P7083, DOI 10.1128/AEM.00557-06; Kabacoff R., 2015, R ACTION DATA ANAL G; Kalbe C, 1996, MICROBIOL RES, V151, P433; Katiyar V, 2004, PLANT GROWTH REGUL, V42, P239, DOI 10.1023/B:GROW.0000026477.10681.d2; Klopper A., 1980, CLIN PHYSL OBSTET, P441; Kumar S, 2016, MOL BIOL EVOL, V33, P1870, DOI 10.1093/molbev/msw054; Laliberte E, 2010, ECOLOGY, V91, P299, DOI 10.1890/08-2244.1; Lane DJ, 1991, NUCL ACID TECHNIQUES, P115; Lauber CL, 2008, SOIL BIOL BIOCHEM, V40, P2407, DOI 10.1016/j.soilbio.2008.05.021; Letunic I, 2011, NUCLEIC ACIDS RES, V39, pW475, DOI 10.1093/nar/gkr201; Lugtenberg B, 2009, ANNU REV MICROBIOL, V63, P541, DOI 10.1146/annurev.micro.62.081307.162918; Lundberg DS, 2012, NATURE, V488, P86, DOI 10.1038/nature11237; Maksimov IV, 2011, APPL BIOCHEM MICRO+, V47, P333, DOI 10.1134/S0003683811040090; Marilley L, 1999, APPL SOIL ECOL, V13, P127, DOI 10.1016/S0929-1393(99)00028-1; Marschner P, 2001, SOIL BIOL BIOCHEM, V33, P1437, DOI 10.1016/S0038-0717(01)00052-9; Masalha J, 2000, BIOL FERT SOILS, V30, P433, DOI 10.1007/s003740050021; Mendes LW, 2015, MICROB ECOL, V70, P255, DOI 10.1007/s00248-014-0559-2; Mendpara J., 2013, EUR J EXP BIOL, V3, P351; Nadeem SM, 2016, ARCH MICROBIOL, V198, P379, DOI 10.1007/s00203-016-1197-5; Nannipieri P, 2003, EUR J SOIL SCI, V54, P655, DOI 10.1046/j.1351-0754.2003.0556.x; O'Toole GA, 1998, MOL MICROBIOL, V30, P295, DOI 10.1046/j.1365-2958.1998.01062.x; Ofek-Lalzar M, 2014, NAT COMMUN, V5, DOI 10.1038/ncomms5950; Olff H, 1997, J ECOL, V85, P799, DOI 10.2307/2960603; Partida-Martinez LP, 2011, FRONT PLANT SCI, V2, DOI 10.3389/fpls.2011.00100; Patten CL, 2002, APPL ENVIRON MICROB, V68, P3795, DOI 10.1128/AEM.68.8.3795-3801.2002; Penrose DM, 2003, PHYSIOL PLANTARUM, V118, P10, DOI 10.1034/j.1399-3054.2003.00086.x; Quast C, 2013, NUCLEIC ACIDS RES, V41, pD590, DOI 10.1093/nar/gks1219; R Core Team, 2013, R LANG ENV STAT COMP; Raaijmakers JM, 2010, FEMS MICROBIOL REV, V34, P1037, DOI 10.1111/j.1574-6976.2010.00221.x; Rasche F, 2006, CAN J MICROBIOL, V52, P1036, DOI 10.1139/W06-059; Rashid S, 2012, APPL SOIL ECOL, V61, P217, DOI 10.1016/j.apsoil.2011.09.011; Ribeiro CM, 2012, MICROBIOL RES, V167, P69, DOI 10.1016/j.micres.2011.03.003; Rosenblueth M, 2006, MOL PLANT MICROBE IN, V19, P827, DOI 10.1094/MPMI-19-0827; Rovira AD, 1956, PLANT SOIL, V7, P178, DOI 10.1007/BF01343726; Saleem M, 2016, MICROB ECOL, V71, P469, DOI 10.1007/s00248-015-0672-x; Salles JF, 2006, MICROB ECOL, V52, P267, DOI 10.1007/s00248-006-9048-6; Salles JF, 2009, ECOLOGY, V90, P3324, DOI 10.1890/09-0188.1; Salles JF, 2017, BIOGEOCHEMISTRY, V132, P185, DOI 10.1007/s10533-017-0296-y; Salles JF, 2012, FRONT MICROBIOL, V3, DOI 10.3389/fmicb.2012.00209; Sasirekha Bakthavatchalu, 2016, Agriculture and Natural Resources, V50, P250, DOI 10.1016/j.anres.2016.02.003; Schnider-Keel U, 2000, J BACTERIOL, V182, P1215, DOI 10.1128/JB.182.5.1215-1225.2000; Schrama M, 2013, PERSPECT PLANT ECOL, V15, P32, DOI 10.1016/j.ppees.2012.12.001; Schrama M, 2012, ECOLOGY, V93, P2353, DOI 10.1890/11-1102.1; SCHULZ BJE, 2006, MICROBIAL ROOT ENDOP, V9, P1, DOI DOI 10.1007/3-540-33526-9; Seoighe C., 2015, ALGORITHMS FRAMEWORK; Sessitsch A, 2002, FEMS MICROBIOL ECOL, V39, P23, DOI [10.1016/S0168-6496(01)00189-1, 10.1111/j.1574-6941.2002.tb00903.x]; Shakya M, 2013, PLOS ONE, V8, DOI 10.1371/journal.pone.0076382; Sharma A, 2003, MICROBIOL RES, V158, P243, DOI 10.1078/0944-5013-00197; Sidhu GS, 1997, ENZYME MICROB TECH, V21, P525, DOI 10.1016/S0141-0229(97)00055-0; Singh BK, 2004, TRENDS MICROBIOL, V12, P386, DOI 10.1016/j.tim.2004.06.008; Smalla K, 2006, FEMS MICROBIOL ECOL, V56, P165, DOI 10.1111/j.1547-6941.2006.00148.x; Smalla K, 2001, APPL ENVIRON MICROB, V67, P4742, DOI 10.1128/AEM.67.10.4742-4751.2001; SMELTZER MS, 1992, APPL ENVIRON MICROB, V58, P2815; Sunagawa S, 2015, SCIENCE, V348, DOI 10.1126/science.1261359; Tavakkoli E, 2011, J EXP BOT, V62, P2189, DOI 10.1093/jxb/erq422; Thompson JD, 1997, NUCLEIC ACIDS RES, V25, P4876, DOI 10.1093/nar/25.24.4876; Timm CM, 2015, FRONT MICROBIOL, V6, DOI 10.3389/fmicb.2015.01118; Turner TR, 2013, GENOME BIOL, V14, DOI 10.1186/gb-2013-14-6-209; Uren N., 2000, RHIZOSPHERE BIOCH OR, P1; Venables B., 2016, POLYNOM COLLECTION F; Versalovic James, 1994, Methods in Molecular and Cellular Biology, V5, P25; Vincent Q. V., 2011, GGBIPLOT GGPLOT2 BAS; Walker L., 2003, PRIMARY SUCCESSION E, DOI [10.1017/CBO9780511615078, DOI 10.1017/CBO9780511615078]; Wang M, 2016, FRONT PLANT SCI, V6, DOI 10.3389/fpls.2015.01188; Wickham H, 2009, USE R, P1, DOI 10.1007/978-0-387-98141-3_1; Yan Y, 2017, ISME J, V11, P56, DOI 10.1038/ismej.2016.108; Yang J, 2009, TRENDS PLANT SCI, V14, P1, DOI 10.1016/j.tplants.2008.10.004; Yilmaz P, 2014, NUCLEIC ACIDS RES, V42, pD643, DOI 10.1093/nar/gkt1209; Zhang HX, 2010, ANN BOT-LONDON, V106, P1027, DOI 10.1093/aob/mcq204
Cited Reference Count 121
Publisher City LAUSANNE
ISSN 1664-302X
29-Character Source Abbreviation FRONT MICROBIOL
ISO Source Abbreviation Front. Microbiol.
Publication Date OCT 30
Year Published 2017
Volume 8
Article Number 2102
Digital Object Identifier (DOI) 10.3389/fmicb.2017.02102
Subject Category 17
Document Delivery Number Microbiology
Unique Article Identifier Microbiology
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