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Mycological Progress

, Volume 17, Issue 11, pp 1213–1224 | Cite as

Rhizoglomus venetianum, a new arbuscular mycorrhizal fungal species from a heavy metal-contaminated site, downtown Venice in Italy

  • Alessandra Turrini
  • Martina Saran
  • Manuela Giovannetti
  • Fritz Oehl
Original Article
  • 195 Downloads

Abstract

Rhizoglomus venetianum, a new arbuscular mycorrhizal fungal species, has been isolated and propagated from a heavy metal-contaminated site in Sacca San Biagio island, downtown Venice, Italy. Interestingly, under the high levels of heavy metals occurring in the site, the new fungus was able to grow only intraradically. In greenhouse trap and single species cultures under low heavy metal levels, the fungus produced innumerous spores, clusters, and sporocarps extraradically, which were formed terminally on subtending hyphae either singly, in small spore clusters, or, preferably, in loose to compact non-organized sporocarps up to 2500 × 2000 × 2000 μm. Spores are golden-yellow to bright yellow brown, globose to subglobose to rarely oblong, 75–145 × 72–140 μm in diameter, and have four spore wall layers. Morphologically, the new fungus is similar to R. intraradices, and phylogenetically, it forms a monophyletic clade next to R. irregulare, which generally forms irregular spores and lacks, like R. intraradices, the flexible innermost wall layer beneath the structural/persistent third wall layer. A key for the species identification is presented comprising all 18 Rhizoglomus species, so far described or newly combined.

Keywords

Arbuscular mycorrhizal fungi Heavy metals Rhizoglomus Morphology Molecular phylogeny SSU–ITS–LSU nrDNA 

Notes

Acknowledgements

The authors thank Stefano Bedini for his technical assistance and Prof. Emanuele Argese for his help in the field.

Author contributions

The work was conceived by M.G. and A.T. A.T. isolated and carried out the trap cultures. M.S. and A.T. carried out the molecular and phylogenetic analysis. F.O. performed the morphological description. A.T., F.O, and M.G. carried out the manuscript preparation for submission. All authors commented on the final draft of the manuscript.

Funding information

The study was financially supported by the University of Pisa (Fondi di Ateneo) and SNF (Bern, projects IZ7370_152740 and IZ76Z0_173895).

References

  1. Abdel-Azeem AM, Abdel-Moneim TS, Ibrahim ME, Hassan MAA, Saleh MY (2007) Effects of long-term heavy metal contamination on diversity of terricolous fungi and nematodes in Egypt-a case study. Wat Air Soil Pollut 186:233–254.  https://doi.org/10.1007/s11270-007-9480-3 CrossRefGoogle Scholar
  2. Alguacil MM, Torrecillas E, Caravaca F, Fernández DA, Azcón R, Roldán A (2011) The application of an organic amendment modifies the arbuscular mycorrhizal fungal communities colonizing native seedlings grown in a heavy-metal-polluted soil. Soil Biol Biochem 43:1498–1508.  https://doi.org/10.1016/j.soilbio.2011.03.026 CrossRefGoogle Scholar
  3. Al-Yahya’ei MN, Mullath SK, AlDhaheri LA, Kozłowska A, Błaszkowski J (2017) Dominikia emiratia and Rhizoglomus dunense, two new species in the Glomeromycota. Botany 95:629–639.  https://doi.org/10.1139/cjb-2016-0294 CrossRefGoogle Scholar
  4. Ban Y, Xu Z, Zhang H, Chen H, Tang M (2015) Soil chemistry properties, translocation of heavy metals, and mycorrhizal fungi associated with six plant species growing on lead–zinc mine. Ann Microbiol 65:503–515.  https://doi.org/10.1007/s13213-014-0886-z CrossRefGoogle Scholar
  5. Bedini S, Turrini A, Rigo C, Argese E, Giovannetti M (2010) Molecular characterization and glomalin production of arbuscular mycorrhizal fungi colonizing a heavy metal polluted ash disposal island, downtown Venice. Soil Biol Biochem 42:758–765.  https://doi.org/10.1016/j.soilbio.2010.01.010 CrossRefGoogle Scholar
  6. Błaszkowski J (2012) Glomeromycota. W. Szafer Institute of Botany, Polish Academy of Sciences, KrakówGoogle Scholar
  7. Błaszkowski J, Chwat G, Góralska A, Ryska P, Kovács GM (2015) Two new genera, Dominikia and Kamienska, and D. disticha sp. nov. In: Glomeromycota. Nova Hedwigia, vol 100, pp 225–238.  https://doi.org/10.1127/nova_hedwigia/2014/0216 CrossRefGoogle Scholar
  8. Błaszkowski J, Kozłowska A, Niezgoda P, Goto BT, Dalpé Y (2018) A new genus, Oehlia with Oehlia diaphana comb. nov. and an emended description of Rhizoglomus vesiculiferum comb. nov. in the Glomeromycotina. Nova Hedwigia, available online.  https://doi.org/10.1127/nova_hedwigia/2018/0488 CrossRefGoogle Scholar
  9. Brundrett M, Melville L, Peterson L (1994) Practical methods in mycorrhizal research. Mycologue Publications, University of Guelph, GuelphGoogle Scholar
  10. Cano C, Bago A, Dalpé Y (2009) Glomus custos sp. nov., isolated from a naturally heavy metal-polluted environment in southern Spain. Mycotaxon 109:499–512.  https://doi.org/10.5248/109.499 CrossRefGoogle Scholar
  11. Clijsters H, Vangronsveld J, van der Lelie N, Colpaert J (2000) Ecological aspects of phytostabilization of heavy metal contaminated soils. In: Ceulemans R, Bogaert J, Deckmyn G, Nijs I (eds) Structure and function in plants and ecosystems. University of Antwerp, UIA, Wilrijk, pp 299–306Google Scholar
  12. Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol Biochem 57:925–928.  https://doi.org/10.1016/j.soilbio.2012.10.031 CrossRefGoogle Scholar
  13. 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 Progress 17:729–744.  https://doi.org/10.1007/s11557-018-1386-5 CrossRefGoogle Scholar
  14. del Mar Montiel-Rozas M, López-García Á, Madejón P, Madejón E (2017) Native soil organic matter as a decisive factor to determine the arbuscular mycorrhizal fungal community structure in contaminated soils. Biol Fertil Soils 53:327–338.  https://doi.org/10.1007/s00374-017-1181-5 CrossRefGoogle Scholar
  15. Ferrol N, González-Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C (2009) Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev 8:551–559.  https://doi.org/10.1007/s11101-009-9133-9 CrossRefGoogle Scholar
  16. Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–246CrossRefGoogle Scholar
  17. Gerdemann JW, Trappe JM (1974) The Endogonaceae in the Pacific Northwest. Mycol Mem 5:1–76Google Scholar
  18. Giovannetti M, Avio L, Salutini L (1990) Morphological, cytochemical, and ontogenetic characteristics of a new species of vesicular-arbuscular mycorrhizal fungus. Can J Bot 69:161–169CrossRefGoogle Scholar
  19. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–594.  https://doi.org/10.1111/j.1469-8137.1993.tb03907.x CrossRefGoogle Scholar
  20. Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122.  https://doi.org/10.1007/s00425-006-0225-0 CrossRefPubMedGoogle Scholar
  21. González-Chávez C, D’Haen J, Vangronsveld J, Dodd JC (2002) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240:287–297.  https://doi.org/10.1023/A:1015794622592 CrossRefGoogle Scholar
  22. González-Chávez MC, Carrillo-Gonzalez R, Gutierrez-Castorena MC (2009) Natural attenuation in a slag heap contaminated with cadmium: the role of plants and arbuscular mycorrhizal fungi. J Hazard Mat 161:1288–1298.  https://doi.org/10.1016/j.jhazmat.2008.04.110 CrossRefGoogle Scholar
  23. Hassan SED, Boon E, St-Arnaud M, Hijiri M (2011) Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol Ecol 20:3469–3483.  https://doi.org/10.1111/j.1365-294X.2011.05142.x CrossRefGoogle Scholar
  24. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146.  https://doi.org/10.1016/j.phytochem.2006.09.023 CrossRefPubMedGoogle Scholar
  25. Khade SW, Adholeya A (2009) Arbuscular mycorrhizal association in plants growing on metal-contaminated and noncontaminated soils adjoining Kanpur tanneries, Uttar Pradesh, India. Wat Air Soil Pollut 202:45–56.  https://doi.org/10.1007/s11270-008-9957-8 CrossRefGoogle Scholar
  26. Koske RE, Tessier B (1983) A convenient, permanent slide mounting medium. Mycol Soc Am Newsl 34:59Google Scholar
  27. Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM (2015) Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One 10:e0128784.  https://doi.org/10.1371/journal.pone.0128784 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223.  https://doi.org/10.1111/j.1469-8137.2009.02835.x CrossRefPubMedGoogle Scholar
  29. Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984.  https://doi.org/10.1111/j.1469-8137.2011.03962.x CrossRefPubMedGoogle Scholar
  30. Long LK, Yao Q, Guo J, Yang RH, Huang YH, Zhu HH (2010) Molecular community analysis of arbuscular mycorrhizal fungi associated with five selected plant species from heavy metal polluted soils. Eur J Soil Biol 46:288–294.  https://doi.org/10.1016/j.ejsobi.2010.06.003 CrossRefGoogle Scholar
  31. Mucina L (1997) Conspectus of classes of European vegetation. Folia Geobot Phytotaxon 32:117–172.  https://doi.org/10.1007/BF02803738 CrossRefGoogle Scholar
  32. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  33. Oehl F, Sieverding E, Palenzuela J, Ineichen K, Alves da Silva G (2011a) Advances in glomeromycota taxonomy and classification. IMA Fungus 2:191–199.  https://doi.org/10.5598/imafungus.2011.02.02.10 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Oehl F, Silva GA, Goto BT, Sieverding E (2011b) Glomeromycota: three new genera, and glomoid species reorganized. Mycotaxon 116:75–120.  https://doi.org/10.5248/116.75 CrossRefGoogle Scholar
  35. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241.  https://doi.org/10.1111/j.1469-8137.2010.03334.x CrossRefPubMedGoogle Scholar
  36. Öpik M, Davison J, Moora M, Zobel M (2014) DNA-based detection and identification of Glomeromycota: the virtual taxonomy of environmental sequences. Botany 92:135–147.  https://doi.org/10.1139/cjb-2013-0110 CrossRefGoogle Scholar
  37. Palenzuela J, Azcón-Aguilar C, Barea JM, Silva GA, Oehl F (2013) Acaulospora pustulata and Acaulospora tortuosa, two new species in the Glomeromycota associated with endangered plants in Sierra Nevada (southern Spain). Nova Hedwigia 97:305–319.  https://doi.org/10.1127/0029-5035/2013/0129 CrossRefGoogle Scholar
  38. Park H, Lee EH, Ka KH, Eom AH (2016) Community structures of arbuscular mycorrhizal fungi in soils and plant roots inhabiting abandoned mines of Korea. Mycobiology 44:277–282.  https://doi.org/10.5941/MYCO.2016.44.4.277 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pawlowska TE, Błaszkowski J, Rühling Å (1996) The mycorrhizal status of plants colonizing a calamine spoil mound in southern Poland. Mycorrhiza 6:499–505.  https://doi.org/10.1007/s005720050154 CrossRefGoogle Scholar
  40. Regvar M, Likar M, Piltaver A, Kugonič N, Smith JE (2010) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil 330:345–356.  https://doi.org/10.1007/s11104-009-0207-7 CrossRefGoogle Scholar
  41. Ronquist F, Teslenko M, Van Der Mark P et al (2012) MrBayes 3.2:efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542.  https://doi.org/10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sánchez-Castro I, Gianinazzi-Pearson V, Cleyet-Marel JC, Baudoin E, van Tuinen D (2017) Glomeromycota communities survive extreme levels of metal toxicity in an orphan mining site. Sci Tot Environ 598:121–128.  https://doi.org/10.1016/j.scitotenv.2017.04.084 CrossRefGoogle Scholar
  43. Schenck NC, Pérez Y (1990) Manual for the identification of VA mycorrhizal fungi, 3rd edn. Synergistic, GainesvilleGoogle Scholar
  44. Sieverding E (1991) Vesicular-arbuscular mycorrhizal management in tropical agrosystems. Deutsche Gesellschaft für Technische Zusammenarbeit 224. Hartmut Bremer Verlag, FriedlandGoogle Scholar
  45. Sieverding E, Silva GA, Berndt R, Oehl F (2014) Rhizoglomus, a new genus in the Glomeraceae. Mycotaxon 129:373–386.  https://doi.org/10.5248/129.373 CrossRefGoogle Scholar
  46. Silva GA, Lumini E, Maia LC, Bonfante P, Bianciotto V (2006) Phylogenetic analysis of Glomeromycota by partial LSU rDNA sequences. Mycorrhiza 16:183–189.  https://doi.org/10.1007/s00572-005-0030-9 CrossRefPubMedGoogle Scholar
  47. Sousa NM, Veresoglou SD, Oehl F, Rillig MC, Maia LC (2018) Predictors of arbuscular mycorrhizal fungal communities in the Brazilian tropical dry forest. Microb Ecol 75:447–458.  https://doi.org/10.1007/s00248-017-1042-7 CrossRefPubMedGoogle Scholar
  48. Spain JL (1990) Arguments for diagnoses based on unaltered wall structures. Mycotaxon 38:71–76Google Scholar
  49. Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474.  https://doi.org/10.1111/j.1469-8137.2010.03262.x CrossRefPubMedGoogle Scholar
  50. Sudová R, Sýkorová Z, Rydlová J, Čtvrtlíková M, Oehl F (2015) Rhizoglomus melanum, a new arbuscular mycorrhizal fungal species associated with submerged plants in freshwater lake Avsjøen in Norway. Mycol Progress 14:9.  https://doi.org/10.1007/s11557-015-1031-5 CrossRefGoogle Scholar
  51. Sun Y, Zhang X, Wu Z, Hu Y, Wu S, Chen B (2016) The molecular diversity of arbuscular mycorrhizal fungi in the arsenic mining impacted sites in Hunan Province of China. J Environ Sci 39:110–118.  https://doi.org/10.1016/j.jes.2015.10.005 CrossRefGoogle Scholar
  52. Symanczik S, Błaszkowski J, Chwat G, Boller T, Wiemken A, Al-Yahya’ei M (2014) Three new species of arbuscular mycorrhizal fungi discovered at one location in a desert of Oman: Diversispora omaniana, Septoglomus nakheelum and Rhizophagus arabicus. Mycologia 106:243–259.  https://doi.org/10.3852/106.2.243 CrossRefPubMedGoogle Scholar
  53. Symanczik S, Al-Yahya’ei MN, Kozłowska A, Ryszka P, Błaszkowski J (2018) A new genus, Desertispora, and a new species, Diversispora sabulosa, in the family Diversisporaceae (order Diversisporales, subphylum Glomeromycotina). Mycol Progress 17:437–449 10.1007%2Fs11557-017-1369-y CrossRefGoogle Scholar
  54. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Tedersoo L, Sánchez-Ramírez S, Urmas Köljalg U, Bahram M, Döring M, Schigel D et al (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fung Div 90:135–159.  https://doi.org/10.1007/s13225-018-0401-0 CrossRefGoogle Scholar
  56. Thaxter R (1922) A revision of the Endogoneae. Proc Amer Acad Arts 57:291–351.  https://doi.org/10.2307/20025921 CrossRefGoogle Scholar
  57. Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174.  https://doi.org/10.1007/s005720000073 CrossRefGoogle Scholar
  58. Turrini A, Giovannetti M (2012) Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation. Mycorrhiza 22:81–97.  https://doi.org/10.1007/s00572-011-0419-6 CrossRefPubMedGoogle Scholar
  59. Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983.  https://doi.org/10.1111/j.1462-2920.2006.00980.x CrossRefPubMedGoogle Scholar
  60. Vogel-Mikuš K, Pongrac P, Kump P, Necemer M, Regvar M (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139:362–371.  https://doi.org/10.1016/j.envpol.2005.05.005 CrossRefPubMedGoogle Scholar
  61. Wei Y, Chen Z, Wu F, Li J, ShangGuan Y, Li F, Zeng QR, Hou H (2015) Diversity of arbuscular mycorrhizal fungi associated with a sb accumulator plant, ramie (Boehmeria nivea), in an active Sb mining. J Microbiol Biotechnol 25:1205–1215.  https://doi.org/10.4014/jmb.1411.11033 CrossRefPubMedGoogle Scholar
  62. Whitfield L, Richards AJ, Rimmer DL (2004) Relationships between soil heavy metal concentration and mycorrhizal colonisation in Thymus polytrichus in northern England. Mycorrhiza 14:55–62.  https://doi.org/10.1007/s00572-003-0268-z CrossRefPubMedGoogle Scholar
  63. Wu FY, Bi YL, Leung HM, Ye ZH, Lin XG, Wong MH (2010) Accumulation of As, Pb, Zn, Cd and Cu and arbuscular mycorrhizal status in populations of Cynodon dactylon grown on metal-contaminated soils. Appl Soil Ecol 44:213–218.  https://doi.org/10.1016/j.apsoil.2009.12.008 CrossRefGoogle Scholar
  64. Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H, Tang M (2015) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158.  https://doi.org/10.1016/j.soilbio.2015.03.018 CrossRefGoogle Scholar
  65. Zarei M, Saleh-Rastin N, Jouzani GS, Savaghebi G, Buscot F (2008) Arbuscular mycorrhizal abundance in contaminated soils around a zinc and lead deposit. E J Soil Biol 44:381–391.  https://doi.org/10.1016/j.ejsobi.2008.06.004 CrossRefGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Alessandra Turrini
    • 1
  • Martina Saran
    • 1
  • Manuela Giovannetti
    • 1
  • Fritz Oehl
    • 2
  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly
  2. 2.Competence Division for Plants and Plant Products, EcotoxicologyAgroscopeWädenswilSwitzerland

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