Symbiosis

, Volume 72, Issue 2, pp 143–152 | Cite as

Arbuscular mycorrhizal fungal diversity in high-altitude hypersaline Andean wetlands studied by 454-sequencing and morphological approaches

  • Vanesa Analía Silvani
  • Roxana Paula Colombo
  • María Victoria Scorza
  • Laura Fernández Bidondo
  • Carolina Paola Rothen
  • Adalgisa Scotti
  • Sebastián Fracchia
  • Alicia Godeas
Article
  • 173 Downloads

Abstract

The Laguna Brava Nature Reserve is a stressful habitat in the Andean Mountains (Argentina) dominated by extreme abiotic factors: high altitude and UV radiance, hypersalinity, alkalinity, and high concentrations of toxic elements in the soil. The sparse native vegetation that inhabits Laguna Brava and Mulas Muertas wetlands is frequently colonized by arbuscular mycorrhizal (AM) fungi. It is, however, unknown which AM species can survive in such a harsh environment and how those environmental conditions influence the AM communities. To answer these questions, 454-amplicon pyrosequencing and morphological (based on spore traits) approaches were used to assess fungal diversity. A total of 23 molecular operational taxonomic units and 14 distinct morphospecies of AM fungi were identified. The morphological characterization of AM fungal communities in Laguna Brava and Mulas Muertas, supported by the molecular data, revealed that Glomeraceae and Claroideoglomeraceae were the dominant families, confirming the predominance of generalist and ruderal AM fungal taxa but with stress-tolerant life history traits. Our results showed that the presence of AM fungi is strongly associated with local environmental variations in Laguna Brava (hypersalinity and high Na+, Sr, As and U contents in soils). The AM fungal communities in Laguna Brava and Mulas Muertas wetlands were similar according to the Simpson diversity index and the ecological distance estimated by Bray Curtis index. These results were also supported by the environmental parameters measured, as they did not vary between the studied sites. This study represents the first characterization of AM fungal community in a high-altitude Andean wetland in Argentina, improving our knowledge about these fungi from extreme environments.

Keywords

Arbuscular mycorrhizal fungi High-altitude wetlands Extreme environment Salinity Heavy metal Pyrosequencing 

Notes

Acknowledgments

We wish to thank to Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Tecnológicas and Agencia Nacional de Promoción Científica y Tecnológica for the financial support, and Secretaría de Ambiente de La Rioja for providing the sampling permission at the Laguna Brava Nature Reserve. We also acknowledge to Dr. Carbonetto María Belén and Dr. Rascován Nicolás (Instituto de Agrobiotecnologia Rosario, INDEAR) for their technical assistance, and Comisión Nacional de Energía Atómica for heavy metals determinations. We appreciate the valuable suggestions of editors and reviewers that have substantially improved our manuscript.

Supplementary material

13199_2016_454_MOESM1_ESM.docx (18 kb)
Supplemental Fig. 1 (DOCX 17 kb)
13199_2016_454_MOESM2_ESM.docx (18 kb)
Supplemental Fig. 2 (DOCX 17 kb)
13199_2016_454_MOESM3_ESM.docx (14 kb)
Supplemental Table 1 (DOCX 13 kb)
13199_2016_454_MOESM4_ESM.docx (14 kb)
Supplemental Table 2 (DOCX 14 kb)

References

  1. Ai-Rong L, Kai-Yun G (2007) Mycorrhizal and dark septate endophytic fungi of Pedicularis species from northwest of Yunnan Province, China. Mycorrhiza 17:103–109CrossRefGoogle Scholar
  2. Appoloni S, Lekberg Y, Tercek MT, Zabinski CA, Redecker D (2008) Molecular community analysis of arbuscular mycorrhizal fungi in roots of geothermal soils in Yellowstone National Park (USA). Microb Ecol 56(4):649–659CrossRefPubMedGoogle Scholar
  3. Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247CrossRefPubMedGoogle Scholar
  4. Becerra A, Bartoloni N, Cofré N, Soteras F, Cabello M (2014) Arbuscular mycorrhizal fungi in saline soils: vertical distribution at different soil depth. Braz J Microbiol 45(2):585–594CrossRefPubMedPubMedCentralGoogle Scholar
  5. Blaszkowski J (2012) Glomeromycota. Koeltz scientific books, Koenigstein, GermanyGoogle Scholar
  6. Bompadre MJ, Pérgola M, Fernández Bidondo L, Colombo RP, Silvani VA, Pardo AG, Ocampo JA, Godeas AM (2014) Evaluation of arbuscular mycorrhizal fungi capacity to alleviate abiotic stress of olive (Olea europaea L.) plants at different transplant conditions. Sci World J Article ID 378950, p12Google Scholar
  7. Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45CrossRefGoogle Scholar
  8. Bremner JM (1996) Nitrogen-total. In: Methods of soil analysis. Part 3-Chemical methods. Soil Science Society of America (Ed), Madison, Wis., USA, pp. 1085–1121.Google Scholar
  9. Campagnac E, Khasa DP (2014) Relationship between genetic variability in Rhizophagus irregularis and tolerance to saline conditions. Mycorrhiza 24:121–129CrossRefPubMedGoogle Scholar
  10. Carrizo R, Baldoni A, Cavallaro S, Dzendoletas MA (1997) Estudio preliminar de las caraterísticas geoambientales del área de reserva Laguna Brava, provincia de La Rioja. Contribuciones Científicas 9:269–281Google Scholar
  11. Chagnon P, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18(9):484–491CrossRefPubMedGoogle Scholar
  12. Colombo RP, Fernández Bidondo L, Silvani VA, Carbonetto MB, Rascovan N, Bompadre MJ, Pérgola M, Cuenca G, Godeas AM (2014) Diversity of arbuscular mycorrhizal fungi in soil from the Pampa Ondulada, Argentina, assessed by pyrosequencing and morphological techniques. Can J Microbiol 60(12):819–827CrossRefPubMedGoogle Scholar
  13. Dai ML, Hamel C, Arnaud MS, He Y, Grant C, Lupwayi N, Janzen H, Malhi SS, Yang XH, Zhou ZQ (2012) Arbuscular mycorrhizal fungi assemblages in Chernozem great groups revealed by massively parallel pyrosequencing. Can J Microbiol 58:81–92CrossRefPubMedGoogle Scholar
  14. del Val C, Barea JM, Azcón-Aguilar C (1999) Assessing the tolerance to heavy metals of arbuscular mycorrhizal fungi isolated from sewage sludge-contaminated soils. Appl Soil Ecol 11:261–269CrossRefGoogle Scholar
  15. Dib JR, Weiss A, Neumann A, Ordoñez O, Estévez MC, Farías ME (2009) Isolation of bacteria from remote high altitude Andean lakes able to grow in the presence of antibiotics. Recent Pat Antiinfect Drug Discov 4(1):66–76CrossRefPubMedGoogle Scholar
  16. Doncaster CC (1962) A counting dish for nematodes. Nematology 7:334–337CrossRefGoogle Scholar
  17. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280CrossRefPubMedPubMedCentralGoogle Scholar
  18. Guo X, Gong J (2014) Differential effects of abiotic factors and host plant traits on diversity and community composition of root-colonizing arbuscular mycorrhizal fungi in a salt-stressed ecosystem. Mycorrhiza 24:79–94CrossRefPubMedGoogle Scholar
  19. Hart M, Reader RJ (2005) The role of the external mycelium in early colonization for three arbuscular mycorrhizal fungal species with different colonization strategies. Pedobiologia 49:269–279CrossRefGoogle Scholar
  20. Klironomos J, Hart M (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184CrossRefPubMedGoogle Scholar
  21. Konstantinidis KT, Tiedje M (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509CrossRefPubMedGoogle Scholar
  22. Lekberg Y, Meadow J, Rohr JR, Redecker D, Zabinski CA (2011) Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. Ecology 92:1292–1302CrossRefPubMedGoogle Scholar
  23. Lentendu G, Zinger L, Manel S, Coissac S, Choler P, Geremia RA, Melodelima C (2011) Assessment of soil fungal diversity in different alpine tundra habitats by means of pyrosequencing. Fungal Divers 49(1):113–123CrossRefGoogle Scholar
  24. Lin X, Feng Y, Zhang H, Chen R, Wang J, Zhang J, Chu H (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ Sci Technol 46(11):5764–5771CrossRefPubMedGoogle Scholar
  25. Liu YJ, He J, Shi G, An L, Öpik M, Feng H (2011) Diverse communities of arbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet plateau. FEMS Microbiol Ecol 78(2):355–365CrossRefPubMedGoogle Scholar
  26. Lugo MA, Ferrero M, Menoyo E, Estevez MC, Sineriz F, Anton A (2008) Arbuscular mycorrhizal fungi and rhizospheric bacteria diversity along an altitudinal gradient in south American puna grassland. Microb Ecol 55(4):705–713CrossRefPubMedGoogle Scholar
  27. Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2009) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12(8):2165–2179PubMedGoogle Scholar
  28. Mendoza RE, García IV, de Cabo L, Weigandt CF, Fabrizio de Iorio A (2015) The interaction of heavy metals and nutrients present in soil and native plants with arbuscular mycorrhizae on the riverside in the Matanza-Riachuelo River Basin (Argentina). Sci Total Environ 505:555–564CrossRefPubMedGoogle Scholar
  29. Oehl F, Schneider D, Sieverding E, Burga CA (2011) Succession of arbuscular mycorrhizal communities in the foreland of the retreating Morteratsch glacier in the Central Alps. Pedobiologia 54:321–331CrossRefGoogle Scholar
  30. Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME, Liira J, Metsis M, Neshataeva V, Paal J, Phosri C, Põlme S, Reier Ü, Saks Ü, Schimann H, Thiéry O, Vasar M, Moora M (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430CrossRefPubMedGoogle Scholar
  31. Rhoades JD, Chanduvi F, Lesch S (1999) Soil salinity assessment – Methods and interpretation of electrical conductivity measurements. In: FAO UNESCO (ed) FAO irrigation and drainage, Rome, pp. 57.Google Scholar
  32. Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strat Gl 9:261–272CrossRefGoogle Scholar
  33. Schechter SP, Bruns TD (2012) Edaphic sorting drives arbuscular mycorrhizal fungal community assembly in a serpentine/non-serpentine mosaic landscape. Ecosphere 3(5):1–24CrossRefGoogle Scholar
  34. Silvani VA, Rothen C, Rodríguez MA, Cisneros G, Godeas A, Aranda-Rickert A, Fracchia S (2013) Fungal root colonization of Puccinellia frigida (Phil.) Johnston, a dominant grass species inhabiting the margins of high-altitude hypersaline Andean wetlands. Aquat Bot 108:26–32CrossRefGoogle Scholar
  35. Silvani VA, Fernández Bidondo L, Bompadre MJ, Pérgola M, Bompadre A, Fracchia S, Godeas AM (2014) Growth dynamics of geographically different arbuscular mycorrhizal fungal isolates belonging to the ‘Rhizophagus clade’ under monoxenic conditions. Mycologia 106(5):963–975CrossRefPubMedGoogle Scholar
  36. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academia Press, Cambridge, UKGoogle Scholar
  37. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  38. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  39. Unterseher M, Jumpponen A, Öpik M, Tedersoo L, Moora M, Dormanns CF, Schnittler M (2011) Species abundance distributions and richness estimations in fungal metagenomic – lesson learned from community ecology. Mol Ecol 20:275–285CrossRefPubMedGoogle Scholar
  40. Walkley A, Black IA (1934) An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–37CrossRefGoogle Scholar
  41. Wang FY, Liu RJ, Lin XG, Zhou JM (2004) Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza 14:133–137CrossRefPubMedGoogle Scholar
  42. Wetzel K, Silva G, Matczinski U, Oehl F, Fester T (2014) Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biol Biochem 72:88–96CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Vanesa Analía Silvani
    • 1
  • Roxana Paula Colombo
    • 1
  • María Victoria Scorza
    • 1
  • Laura Fernández Bidondo
    • 1
  • Carolina Paola Rothen
    • 1
  • Adalgisa Scotti
    • 2
  • Sebastián Fracchia
    • 3
  • Alicia Godeas
    • 1
  1. 1.Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, IBBEA-CONICETUniversidad de Buenos Aires, Ciudad UniversitariaBuenos AiresArgentina
  2. 2.International Center for Earth Sciences, Regional Mendoza, Comisión Nacional de Energía AtómicaMendozaArgentina
  3. 3.Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La RiojaCRILAR- CONICETAnillacoArgentina

Personalised recommendations