Abstract
The ecological restoration of nickel mining-degraded areas in New Caledonia is strongly limited by low availability of soil mineral nutrients, metal toxicity, and slow growth rates of native plant species. In order to improve plant growth for restoration programs, special attention was paid to interactions between plant and soil microorganisms. In this study, we evaluated the influence of inoculation with Curtobacterium citreum BE isolated from a New Caledonian ultramafic soil on arbuscular mycorrhizal symbiosis and growth of Tetraria comosa, an endemic sedge used in restoration programs. A greenhouse experiment on ultramafic substrate was conducted with an inoculum comprising two arbuscular mycorrhizal fungi (AMF) species isolated from New Caledonian ultramafic soils: Rhizophagus neocaledonicus and Claroideoglomus etunicatum. The effects on plant growth of the AMF and C. citreum BE inoculated separately were not significant, but their co-inoculation significantly enhanced the dry weight of T. comosa compared with the non-inoculated control. These differences were positively correlated with mycorrhizal colonization which was improved by C. citreum BE. Compared with the control, co-inoculated plants were characterized by better mineral nutrition, a higher Ca/Mg ratio, and lower metal translocation. However, for Ca/Mg ratio and metal translocation, there were no significant differences between the effects of AMF inoculation and co-inoculation.
Similar content being viewed by others
References
Amir H, Pineau R, Violette Z (1997) Premiers résultats sur les endomycorhizes des plantes de maquis miniers. In: Jaffré T, Reeves RD, Becquer T (eds) The ecology of ultramafic and metalliferous areas. ORSTOM Edi. Noumea, New Caledonia, pp 79–85
Amir H, Jasper DA, Abbott LK (2008) Tolerance and induction of tolerance to Ni of arbuscular mycorrhizal fungi from New Caledonian ultramafic soils. Mycorrhiza 19:1–6. https://doi.org/10.1007/s00572-008-0197-y
Amir H, Jourand P, Cavaloc Y, Ducousso M (2014) Role of mycorrhizal fungi on the alleviation of heavy metal toxicity on plant. In: Zakaria M. Solaiman; Lynette K. Abbott; Ajit Varma (eds.) Mycorrhizal fungi : use in sustainable agriculture and land restoration. New-York: Springer 241–258. https://link.springer.com/chapter/10.1007/978-3-662-45370-4_15
Amir H, Cavaloc Y, Laurent A, Pagand P, Gunkel P, Lemestre M, Médevielle V, Pain A, McCoy S (2019) Arbuscular mycorrhizal fungi and sewage sludge enhance growth and adaptation of Metrosideros laurifolia on ultramafic soil in New Caledonia: a field experiment. Sci Total Environ 651:334–343. https://doi.org/10.1016/j.scitotenv.2018.09.153
Barea J-M, Azcón R, Azcón-Aguilar C (2002a) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81:343–351. https://doi.org/10.1023/A:1020588701325
Barea JM, Toro M, Orozco MO et al (2002b) The application of isotopic (32P and15N) dilution techniques to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops. Nutr Cycl Agroecosyst 63:35–42. https://doi.org/10.1023/A:1020589732436
Battini F, Grønlund M, Agnolucci M, Giovannetti M, Jakobsen I (2017) Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci Rep 7:4686. https://doi.org/10.1038/s41598-017-04959-0
Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996a) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010
Bianciotto V, Minerdi D, Perotto S, Bonfante P (1996b) Cellular interactions between arbuscular mycorrhizal fungi and rhizosphere bacteria. Protoplasma 193:123–131. https://doi.org/10.1007/BF01276640
Bianciotto V, Andreotti S, Balestrini R et al (2001) Extracellular polysaccharides are involved in the attachment of Azospirillum brasilense and Rhizobium leguminosarum to arbuscular mycorrhizal structures. Eur J Histochem 45:39–49. https://doi.org/10.4081/1612
Bidondo LF, Silvani V, Colombo R et al (2011) Pre-symbiotic and symbiotic interactions between Glomus intraradices and two Paenibacillus species isolated from AM propagules. In vitro and in vivo assays with soybean (AG043RG) as plant host. Soil Biol Biochem 43:1866–1872. https://doi.org/10.1016/j.soilbio.2011.05.004
Bonfante P, Anca I (2009) Plants , mycorrhizal fungi , and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. https://doi.org/10.1146/annurev.micro.091208.073504
Borkott H, Insam H (1990) Symbiosis with bacteria enhances the use of chitin by the springtail, Folsomia candida (Collembola). Biol Fertil Soils 9:126–129. https://doi.org/10.1007/BF00335794
Bourles A, Guentas L, Chalkiadakis E, Majorel C, Juillot F, Cavaloc Y, Burtet-Sarramegna V, Medevielle V, Jourand P, Amir H (2019) New Caledonian ultramafic conditions structure the features of Curtobacterium citreum strains that play a role in plant adaptation. Can J Microbiol 65:880–894. https://doi.org/10.1139/cjm-2019-0283
Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266. https://doi.org/10.1146/annurev.ecolsys.35.021103.105730
Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscoride, Portland, OR
Brundrett M, Tedersoo L (2019) Misdiagnosis of mycorrhizas and inappropriate recycling of data can lead to false conclusions. New Phytol 221:18–24. https://doi.org/10.1111/nph.15440
Crossay T (2018) Caractérisation taxonomique des champignons mycorhiziens à arbuscules natifs des sols ultramafiques de Nouvelle-Calédonie; analyse de leur synergie permettant l’adaptation des plantes à ces milieux extrêmes. PhD thesis, New Caledonia University
Crossay T, Cilia A, Cavaloc Y, Amir H, Redecker D (2018) Four new species of arbuscular mycorrhizal fungi (Glomeromycota) associated with endemic plants from ultramafic soils of New Caledonia. Mycol Prog 17:729–744. https://doi.org/10.1007/s11557-018-1386-5
Crossay T, Majorel C, Redecker D, Gensous S, Medevielle V, Durrieu G, Cavaloc Y, Amir H (2019) Is a mixture of arbuscular mycorrhizal fungi better for plant growth than single-species inoculants? Mycorrhiza 29:325–339. https://doi.org/10.1007/s00572-019-00898-y
Daniels BA, Skipper HD (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck NC (ed) Methods and principles of Mycorrhizal research. The American Phytopath Society, St Paul, Minnesota, U.S.A, pp 29–35
Doubková P, Sudová R (2014) Nickel tolerance of serpentine and non-serpentine Knautia arvensis plants as affected by arbuscular mycorrhizal symbiosis. Mycorrhiza 24:209–217. https://doi.org/10.1007/s00572-013-0532-9
Doubková P, Suda J, Sudová R (2011) Arbuscular mycorrhizal symbiosis on serpentine soils: the effect of native fungal communities on different Knautia arvensis ecotypes. Plant Soil 345:325–338. https://doi.org/10.1007/s11104-011-0785-z
Etesami H (2018) Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol Environ Saf 147:175–191. https://doi.org/10.1016/j.ecoenv.2017.08.032
Fernández Bidondo L, Colombo R, Bompadre J et al (2016) Cultivable bacteria associated with infective propagules of arbuscular mycorrhizal fungi. Implications for mycorrhizal activity. Appl Soil Ecol 105:86–90. https://doi.org/10.1016/j.apsoil.2016.04.013
Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x
Gamalero E, Lingua G, Berta G, Glick BR (2009) Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can J Microbiol 55:501–514. https://doi.org/10.1139/w09-010
Garbaye J (1994) Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210. https://doi.org/10.1111/j.1469-8137.1994.tb04003.x
Gonin M, Gensous S, Lagrange A, Ducousso M, Amir H, Jourand P (2013) Rhizosphere bacteria of Costularia spp. from ultramafic soils in New Caledonia: diversity, tolerance to extreme edaphic conditions, and role in plant growth and mineral nutrition. Can J Microbiol 59:164–174. https://doi.org/10.1139/cjm-2012-0570
Guentas L, Gensous S, Cavaloc Y, Ducousso M, Amir H, de Georges de Ledenon B, Moulin L, Jourand P (2016) Burkholderia novacaledonica sp. nov. and B. ultramafica sp. nov. isolated from roots of Costularia spp. pioneer plants of ultramafic soils in New Caledonia. Syst Appl Microbiol 39:151–159. https://doi.org/10.1016/j.syapm.2016.03.008
Iffis B, St-Arnaud M, Hijri M (2014) Bacteria associated with arbuscular mycorrhizal fungi within roots of plants growing in a soil highly contaminated with aliphatic and aromatic petroleum hydrocarbons. FEMS Microbiol Lett 358:44–54. https://doi.org/10.1111/1574-6968.12533
Isnard S, L’Huillier L, Rigault F, Jaffré T (2016) How did the ultramafic soils shape the flora of the new Caledonian hotspot? Plant Soil 403:53–76. 5. https://doi.org/10.1007/s11104-016-2910-5
Jaffré T (1992) Floristic and ecological diversity of the vegetation on ultramafic rocks in New Caledonia. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 101–107
Jaffré T, L’Huillier L (2010a) La végétation des roches ultramafiques ou terrains miniers. In: L’Huillier L, Jaffré T, Wulff A (eds) Mines et environnement en Nouvelle-Calédonie : les milieux sur substrats ultramafiques et leur restauration. IAC Ed, Noumea, pp 45–103
Jaffré T, L’huillier L (2010b) Conditions de milieu des terrains miniers. In: L’Huillier L, Jaffré T, Wulff A (eds) Mines et environnement en Nouvelle-Calédonie : les milieux sur substrats ultramafiques et leur restauration. IAC Ed, Noumea, pp 33–44
Kazakou E, Dimitrakopoulos PG, Baker AJM et al (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev:495–508. https://doi.org/10.1111/j.1469-185X.2008.00051.x
Koele N, Turpault MP, Hildebrand EE et al (2009) Interactions between mycorrhizal fungi and mycorrhizosphere bacteria during mineral weathering: budget analysis and bacterial quantification. Soil Biol Biochem 41:1935–1942. https://doi.org/10.1016/j.soilbio.2009.06.017
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488. https://doi.org/10.1016/S0953-7562(89)80195-9
Koske RE, Gemma JN (1997) Mycorrhizae and succession in plantings of beachgrass in sand dunes. Am J Bot 84:118–130. https://doi.org/10.2307/2445889
Lagrange A, Ducousso M, Jourand P, Majorel C, Amir H (2011) New insights into the mycorrhizal status of Cyperaceae from ultramafic soils in New Caledonia. Can J Microbiol 57:21–28. https://doi.org/10.1139/W10-096
Lagrange A, L’Huillier L, Amir H (2013) Mycorrhizal status of Cyperaceae from New Caledonian ultramafic soils: effects of phosphorus availability on arbuscular mycorrhizal colonization of Costularia comosa under field conditions. Mycorrhiza 23:655–661. https://doi.org/10.1007/s00572-013-0503-1
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient Acquisition of Phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Larcher M, Muller B, Mantelin S et al (2003) Early modifications of Brassica napus root system architecture induced by a plant growth-promoting Phyllobacterium strain. New Phytol 160:119–125. https://doi.org/10.1046/j.1469-8137.2003.00862.x
Larridon I, Bauters K, Semmouri I, Viljoen JA, Prychid CJ, Muasya AM, Bruhl JJ, Wilson KL, Senterre B, Goetghebeur P (2018) Molecular phylogenetics of the genus Costularia (Schoeneae, Cyperaceae) reveals multiple distinct evolutionary lineages. Mol Phylogenet Evol 126:196–209. https://doi.org/10.1016/j.ympev.2018.04.016
Long L, Lin Q, Yao Q, Zhu H (2017) Population and function analysis of cultivable bacteria associated with spores of arbuscular mycorrhizal fungus Gigaspora margarita. 3 Biotech 7:4–9. https://doi.org/10.1007/s13205-017-0612-1
Miransari M (2011) Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl Microbiol Biotechnol 89:917–930. https://doi.org/10.1007/s00253-010-3004-6
Orłowska E, Przybyłowicz W, Orlowski D, Turnau K, Mesjasz-Przybyłowicz J (2011) The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environ Pollut 159:3730–3738. https://doi.org/10.1016/j.envpol.2011.07.008
Perrier N, Amir H, Colin F (2006) Occurrence of mycorrhizal symbioses in the metal-rich lateritic soils of the Koniambo massif, New Caledonia. Mycorrhiza 16:449–458. https://doi.org/10.1007/s00572-006-0057-6
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/ Accessed Dec 2018
Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Selvakumar G, Krishnamoorthy R, Kim K, Sa T-M (2016) Genetic diversity and association characters of bacteria isolated from arbuscular mycorrhizal fungal spore walls. PLoS One 11:e0160356. https://doi.org/10.1371/journal.pone.0160356
Selvakumar G, Shagol CC, Kim K, Han S, Sa T (2018) Spore associated bacteria regulates maize root K+/Na+ ion homeostasis to promote salinity tolerance during arbuscular mycorrhizal symbiosis. BMC Plant Biol 18:109. https://doi.org/10.1186/s12870-018-1317-2
Smith SE, Read D (2008) Mycorrhizal symbiosis. 3rd Edition, Academic press, London. https://doi.org/10.1016/B978-0-12-370526-6.X5001-6
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Taktek S, Trépanier M, Servin PM et al (2015) Trapping of phosphate solubilizing bacteria on hyphae of the arbuscular mycorrhizal fungus Rhizophagus irregularis DAOM 197198. Soil Biol Biochem 90:1–9. https://doi.org/10.1016/j.soilbio.2015.07.016
Tarkka MT, Frey-Klett P (2008) Mycorrhiza helper bacteria. In: Mycorrhiza. Springer, Berlin, Heidelberg, pp 113–132
Trouvelot A, Kough J, Gianinazi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi_Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221
Turrini A, Avio L, Giovannetti M, Agnolucci M (2018) Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of translational research. Front Plant Sci 9:10–13. https://doi.org/10.3389/fpls.2018.01407
Vacheron J, Desbrosses G, Bouffaud M-L, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. https://doi.org/10.3389/fpls.2013.00356
Vivas A, Barea JM, Biro B, Azcon R (2006a) Effectiveness of autochthonous bacterium and mycorrhizal fungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminated soil. J Appl Microbiol 100:587–598. https://doi.org/10.1111/j.1365-2672.2005.02804.x
Vivas A, Biró B, Ruíz-Lozano JM et al (2006b) Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62:1523–1533. https://doi.org/10.1016/j.chemosphere.2005.06.053
Xie L, Lehvävirta S, Timonen S, Kasurinen J, Niemikapee J, Valkonen JPT (2018) Species-specific synergistic effects of two plant growth—promoting microbes on green roof plant biomass and photosynthetic efficiency. PLoS One 13:e0209432. https://doi.org/10.1371/journal.pone.0209432
Yousefi AA, Khavazi K, Moezi AA et al (2011) Phosphate solubilizing bacteria and arbuscular mycorrhizal fungi impacts on inorganic phosphorus fractions and wheat growth. World Appl Sci J 15:1310–1318
Acknowledgments
The authors thank the LAMA laboratory (LAMA-US IMAGO-IRD, New Caledonia) for chemical analyses and M. Voide for technical support.
Funding
We are very grateful to the South Province of New Caledonia for providing the PhD grant of Alexandre Bourles. This work was supported by the Province Sud of New Caledonia (Prix d’Encouragement à la Recherche: Thesis Grant).
Author information
Authors and Affiliations
Contributions
A.B. designed the study, performed the research, analyzed the data, and wrote the paper; L.G. designed the study and wrote the paper; C.C. performed the research and analyzed the data; S.G analyzed the data; C.M. performed the research; T.C. provided AMF inoculum, designed the study, and wrote the paper; Y.C. designed the study; V.B.S. wrote the paper and provided the funding; P.J. designed the study and wrote the paper; H.A. supervised the study, analyzed the data, wrote the manuscript, and provided the funding.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 427 kb)
Rights and permissions
About this article
Cite this article
Bourles, A., Guentas, L., Charvis, C. et al. Co-inoculation with a bacterium and arbuscular mycorrhizal fungi improves root colonization, plant mineral nutrition, and plant growth of a Cyperaceae plant in an ultramafic soil. Mycorrhiza 30, 121–131 (2020). https://doi.org/10.1007/s00572-019-00929-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-019-00929-8