Abstract
Hydrocarbon pollution is an increasing problem affecting soil ecosystems. However, some microorganisms can cope with these pollutants and even facilitate plant establishment and thus phytoremediation. Within soil, arbuscular mycorrhizal fungi (AMF) have developed several strategies to survive and flourish under adverse conditions. Among these is the hyphal healing mechanism (HHM), a process allowing hyphae to re-establish integrity after physical injury. This mechanism differs among species and genera of AMF. However, whether and to what extent hydrocarbon pollution impacts the HHM is unknown. Here, the HHM was monitored in vitro on two AMF strains, Rhizophagus irregularis MUCL 41833 and Gigaspora sp. MUCL 52331, under increasing concentrations of diesel (1, 2, and 5% v:v). The addition of diesel slowed-down the HHM in both fungi. On Gigaspora sp., this effect was limited and most hyphae were able to heal after injury. Conversely, all steps of healing were severely impaired in R. irregularis. That fungus reconnected the injured hyphae at a much lower frequency than the Gigaspora sp., instead investing its energy to link neighboring hyphae or roots, or developing new branches from uninjured hyphae.
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References
Abha S, Singh CS (2012) Hydrocarbon pollution: effects on living organisms, remediation of contaminated environments, and effects of heavy metals co-contamination on bioremediation. Introd to Enhanc Oil Recover Process Bioremediat Oil-Contaminated Sites 21:185–206. https://doi.org/10.5772/48014
Adam G, Duncan H (1999) Effect of diesel fuel on growth of selected plant species. Environ Geochem Health 21:353–357
Amadi A, Abbey SD, Nma A (1996) Chronic effects of oil spill on soil properties and microflora of a rainforest ecosystem in Nigeria. Water Air Soil Pollut 86:1–11. https://doi.org/10.1007/BF00279142
Cabello MN (1999) Effectiveness of indigeneous arbuscular mycorrhizal fungi (AMF) isolated from hydrocarbon polluted soils. Basic Microbiol 39:89–95
Calonne-Salmon M, Plouznikoff K, Declerck S (2018) The arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833 increases the phosphorus uptake and biomass of Medicago truncatula, a benzo[a]pyrene-tolerant plant species. Mycorrhiza 28:761–771. https://doi.org/10.1007/s00572-018-0861-9
Calonne M, Fontaine J, Debiane D et al (2014a) Impact of anthracene on the arbuscular mycorrhizal fungus lipid metabolism1. Botany 92:173–178. https://doi.org/10.1139/cjb-2013-0094
Calonne M, Fontaine J, Debiane D et al (2014b) The arbuscular mycorrhizal Rhizophagus irregularis activates storage lipid biosynthesis to cope with the benzo[a]pyrene oxidative stress. Phytochemistry 97:30–37. https://doi.org/10.1016/j.phytochem.2013.10.014
Cox DR (1972) Regression Models and Life-Tables. J R Stat Soc Ser B 34:187–202. https://doi.org/10.1111/j.2517-6161.1972.tb00899.x
Cranenbrouck S, Voets L, Bivort C et al (2005) Methodologies for in vitro cultivation of arbuscular mycorrhizal fungi with root organs. In: Declerck S, Strullu D, Fortin J (eds) In vitro culture of mycorrhizas. Springer, Berlin Heidelberg, Berlin, pp 341–348
Dalpé Y, Trépanier M, Lounès-Hadj Sahraoui A et al (2012) Lipids of Mycorrhizas. In: Hock B (ed) Fungal Associations, The Mycota IX, 2nd edn. Springer-Verlag, Berlin Heidelberg, pp 137–169
de la Providencia IE, de Souza FA, Fernández F et al (2005) Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis formation and hyphal healing mechanisms between different phylogenic groups. New Phytol 165:261–271. https://doi.org/10.1128/AEM.69.7.4308-4311.2003
de la Providencia IE, Fernández F, Declerck S (2007) Hyphal healing mechanism in the arbuscular mycorrhizal fungi Scutellospora reticulata and Glomus clarum differs in response to severe physical stress. FEMS Microbiol Lett 268:120–125. https://doi.org/10.1111/j.1574-6968.2006.00572.x
de Novais CB, Avio L, Giovannetti M et al (2019) Interconnectedness, length and viability of arbuscular mycorrhizal mycelium as affected by selected herbicides and fungicides. Appl Soil Ecol 143:144–152. https://doi.org/10.1016/j.apsoil.2019.06.013
de Novais CB, Pepe A, Siqueira JO et al (2017) Compatibility and incompatibility in hyphal anastomosis of arbuscular mycorrhizal fungi. Sci Agric 74:411–416. https://doi.org/10.1590/1678-992x-2016-0243
de Souza FA, Declerck S (2003) Mycelium development and architecture, and spore production of Scutellospora reticulata in monoxenic culture with Ri T-DNA transformed carrot roots. Mycologia 95:1004–1012. https://doi.org/10.1080/15572536.2004.11833016
Debiane D, Calonne M, Fontaine J et al (2011) Lipid content disturbance in the arbuscular mycorrhizal, Glomus irregulare grown in monoxenic conditions under PAHs pollution. Fungal Biol 115:782–792. https://doi.org/10.1016/j.funbio.2011.06.003
Debiane D, Garçon G, Verdin A et al (2008) In vitro evaluation of the oxidative stress and genotoxic potentials of anthracene on mycorrhizal chicory roots. Environ Exp Bot 64:120–127. https://doi.org/10.1016/j.envexpbot.2008.04.003
Debiane D, Garçon G, Verdin A et al (2009) Mycorrhization alleviates benzo[a]pyrene-induced oxidative stress in an in vitro chicory root model. Phytochemistry 70:1421–1427. https://doi.org/10.1016/j.phytochem.2009.07.002
Declerck S, Strullu DG, Plenchette C (1998) Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90:579–585. https://doi.org/10.2307/3761216
Delord M (2015) MIICD: data augmentation and multiple imputation for interval censored data. R Libr. https://doi.org/10.13140/RG.2.1.2084.8168
Dorn PB, Salanitro JP (2000) Temporal ecological assessment of oil contaminated soils before and after bioremediation. Chemosphere 40:419–426. https://doi.org/10.1016/S0045-6535(99)00304-5
Driai S, Verdin A, Laruelle F et al (2015) Is the arbuscular mycorrhizal fungus Rhizophagus irregularis able to fulfil its life cycle in the presence of diesel pollution? Int Biodeterior Biodegrad 105:58–65. https://doi.org/10.1016/j.ibiod.2015.08.012
Faure D, Bonin P, Duran R (2015) Environmental microbiology as a mosaic of explored ecosystems and issues. Environ Sci Pollut Res 22:13577–13598. https://doi.org/10.1007/s11356-015-5164-5
Fontaine J, Grandmougin-Ferjani A, Glorian V, Durand R (2004) 24-Methyl/methylene sterols increase in monoxenic roots after colonization by arbuscular mycorrhizal fungi. New Phytol 163:159–167. https://doi.org/10.1111/j.1469-8137.2004.01075.x
Franco-Ramírez A, Ferrera-Cerrato R, Varela-Fregoso L et al (2007) Arbuscular mycorrhizal fungi in chronically petroleum-contaminated soils in Mexico and the effects of petroleum hydrocarbons on spore germination. J Basic Microbiol 47:378–383
Gan S, Lau EV, Ng HK (2009) Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549. https://doi.org/10.1016/j.jhazmat.2009.07.118
George B, Seals S, Aban I (2014) Survival analysis and regression models. J Nucl Cardiol 21:686–694. https://doi.org/10.1007/s12350-014-9908-2
Giovannetti M, Avio L, Sbrana C (2015) Functional significance of anastomosis in arbuscular mycorrhizal networks. In: Horton TR (ed) Mycorrhizal Networks. Ecological Studies, Springer Science+Business, pp 41–68
Giovannetti M, Azzolini D, Citernesi AS (1999) Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl Environ Microbiol 65:5571–5575
Giovannetti M, Fortuna P, Citernesi AS et al (2001) The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 151:717–724. https://doi.org/10.1046/j.0028-646x.2001.00216.x
Giovannetti M, Sbrana C, Avio L, Strani P (2004) Patterns of below-ground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 164:175–181. https://doi.org/10.1111/j.1469-8137.2004.01145.x
IJdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21:1–16
ISO (International-Organization-for-Standardization) (2009) ISO/TS 10832: Soil quality — Effects of pollutants on mycorrhizal fungi — Spore germination test. In: ISO/TS 10832. https://www.iso.org/obp/ui/#iso:std:iso:ts:10832:ed-1:v2:en. Accessed 27 Jul 2020
Joner EJ, Leyval C (2001) Influence of arbuscular mycorrhiza on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10:155–159. https://doi.org/10.1007/s005720000071
Joye SB, Teske AP, Kostka JE (2014) Microbial dynamics following the macondo oil well blowout across gulf of Mexico environments. Bioscience 64:766–777. https://doi.org/10.1093/biosci/biu121
Kauppi S, Sinkkonen A, Romantschuk M (2011) Enhancing bioremediation of diesel-fuel-contaminated soil in a boreal climate: Comparison of biostimulation and bioaugmentation. Int Biodeterior Biodegrad 65:359–368. https://doi.org/10.1016/j.ibiod.2010.10.011
Kirk JL, Moutoglis P, Klironomos J et al (2005) Toxicity of diesel fuel to germination, growth and colonization of Glomus intraradices in soil and in vitro transformed carrot root cultures. Plant Soil 270:23–30. https://doi.org/10.1007/s11104-004-1013-x
Kirk P, Cannon PF, David J, Stalpers J (2001) Ainsworth and Bisby’s Dictionary of the Fungi, 9th edn. CABI, Wallingford, UK
Kokkoris V, Stefani F, Dalpé Y et al (2020) Nuclear dynamics in the arbuscular mycorrhizal fungi. Trends Plant Sci 25:765–778. https://doi.org/10.1016/j.tplants.2020.05.002
Lenoir I, Fontaine J, Tisserant B et al (2017) Beneficial contribution of the arbuscular mycorrhizal fungus, Rhizophagus irregularis, in the protection of Medicago truncatula roots against benzo[a]pyrene toxicity. Mycorrhiza 27:465–476. https://doi.org/10.1007/s00572-017-0764-1
Lenoir I, Lounes-Hadj Sahraoui A, Fontaine J (2016) Arbuscular mycorrhizal fungal-assisted phytoremediation of soil contaminated with persistent organic pollutants: a review. Eur J Soil Sci 67:624–640. https://doi.org/10.1111/ejss.12375
Leyval C, Binet P (1998) Effect of polyaromatic hydrocarbons in soil on arbuscular mycorrhizal plants. J Environ Qual 27:402–407. https://doi.org/10.2134/jeq1998.00472425002700020022x
Liang F, Lu M, Keener TC et al (2005) The organic composition of diesel particulate matter, diesel fuel and engine oil of a non-road diesel generator. J Environ Monit 7:983–988. https://doi.org/10.1039/b504728e
Logi C, Sbrana C, Giovannetti M (1998) Cellular events involved in survival of individual arbuscular mycorrhizal symbionts growing in the absence of the host. Appl Environ Microbiol 64:3473–3479
Meglouli H, Fontaine J, Verdin A et al (2019) Aided phytoremediation to clean up dioxins/furans-aged contaminated soil: Correlation between microbial communities and pollutant dissipation. Microorganisms 7:1–18. https://doi.org/10.3390/microorganisms7110523
Merkl N, Schultze-Kraft R, Infante C (2005) Phytoremediation in the tropics—influence of heavy crude oil on root morphological characteristics of graminoids. Environ Pollut 138:86–91. https://doi.org/10.1016/j.envpol.2005.02.023
Nicolotti G, Egli S (1998) Soil contamination by crude oil: Impact on the mycorrhizosphere and on the revegetation potential of forest trees. Environ Pollut 99:37–43. https://doi.org/10.1016/S0269-7491(97)00179-6
Nwoko CO (2014) Effect of arbuscular mycorrhizal (AM) fungi on the physiological performance of phaseolus vulgaris grown under crude oil contaminated soil. J Geosci Environ Prot 2:9–14. https://doi.org/10.4236/gep.2014.24002
Peng M, Zi X, Wang Q (2015) Bacterial community diversity of oil-contaminated soils assessed by high throughput sequencing of 16s rRNA genes. Int J Environ Res Public Health 12:12002–12015. https://doi.org/10.3390/ijerph121012002
Plouznikoff K, Declerck S, Calonne-Salmon M (2016) Mitigating abiotic stresses in crop plants by arbuscular mycorrhizal fungi. In: Vos CMF, Kazan K (eds) Belowground Defence Strategies in Plants. Springer International Publishing Switzerland, Signaling and Communication in Plants, pp 341–400
Purin S, Morton JB (2011) In situ analysis of anastomosis in representative genera of arbuscular mycorrhizal fungi. Mycorrhiza 21:505–514. https://doi.org/10.1007/s00572-010-0356-9
Rajtor M, Piotrowska-Seget Z (2016) Prospects for arbuscular mycorrhizal fungi (AMF) to assist in phytoremediation of soil hydrocarbon contaminants. Chemosphere 162:105–116. https://doi.org/10.1016/j.chemosphere.2016.07.071
Salami AO, Elum EA (2010) Bioremediation of a crude oil polluted soil with Pleurotus pulmonarius and Glomus mosseae using Amaranthus hybridus as a test plant. J Bioremediation Biodegrad 01. https://doi.org/10.4172/2155-6199.1000113
Sbrana C, Fortuna P, Giovannetti M (2011) Plugging into the network: belowground connections between germlings and extraradical mycelium of arbuscular mycorrhizal fungi. Mycologia 103:307–316. https://doi.org/10.3852/10-125
Simard SW, Beiler KJ, Bingham MA et al (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60. https://doi.org/10.1016/j.fbr.2012.01.001
Stefani FOP, Bell TH, Marchand C et al (2015) Culture-dependent and -independent methods capture different microbial community fractions in hydrocarbon-contaminated soils. PLoS One 10:e0128272. https://doi.org/10.1371/journal.pone.0128272
Tang M, Chen H, Huang JC, Tian ZQ (2009) AM fungi effects on the growth and physiology of Zea mays seedlings under diesel stress. Soil Biol Biochem 41:936–940. https://doi.org/10.1016/j.soilbio.2008.11.007
Vanden Bossche H (1990) Importance and role of sterols in fungal membranes. In: Kuhn PJ, Trinci APJ, Jung MJ, Goosey MW, Copping LG (ed) Biochemistry of Cell Walls and Membranes in Fungi. Springer-Verlag, Berlin, pp 135–157
Verdin A, Lounès-Hadj Sahraoui A, Fontaine J et al (2006) Effects of anthracene on development of an arbuscular mycorrhizal fungus and contribution of the symbiotic association to pollutant dissipation. Mycorrhiza 16:397–405. https://doi.org/10.1007/s00572-006-0055-8
Voets L, de la Providencia IE, Declerck S (2006) Glomeraceae and Gigasporaceae differ in their ability to form hyphal networks. New Phytol 172:185–188. https://doi.org/10.1111/j.1469-8137.2006.01873.x
Voets L, de la Providencia IE, Fernandez K et al (2009) Extraradical mycelium network of arbuscular mycorrhizal fungi allows fast colonization of seedlings under in vitro conditions. Mycorrhiza 19:347–356. https://doi.org/10.1007/s00572-009-0233-6
Vwioko DE, Omamogho CE (2012) Assessing successive plant growth on petroleum hydrocarbon degradation in highly polluted soil augmented with wood ash. Int J Appl Sci Technol 2:247–267
Weete JD (1989) Structure and function of sterols in fungi. Adv Lipid Res 23:115–167
Funding
This research was sponsored by the CIUF–CUD (currently ARES, Académie de Recherche et d’enseignement Supérieur Wallonie-Bruxelles, Commission de la Coopération pour le Dévelopment CIUF) through the PIC Project entitled “Reinforcement of the fungal expertise in Ecuador via case studies of fungal plants interactions in selected ecosystems and the development of biotechnology-oriented fungal resource.” Additional support was given to Mónica Garcés Ruiz by the Pontificia Universidad Católica del Ecuador (PUCE) projects.
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Garcés-Ruiz, M., Calonne-Salmon, M., Bremhorst, V. et al. Diesel fuel differentially affects hyphal healing in Gigaspora sp. and Rhizophagus irregularis. Mycorrhiza 31, 413–421 (2021). https://doi.org/10.1007/s00572-021-01026-5
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DOI: https://doi.org/10.1007/s00572-021-01026-5