Advertisement

Mycorrhiza

, Volume 28, Issue 7, pp 587–603 | Cite as

Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns

  • Sidney L. Stürmer
  • James D. Bever
  • Joseph B. Morton
Original Article

Abstract

Information on the biogeography of arbuscular mycorrhizal fungi (AMF) is important because this group of obligately symbiotic soil microbes is a ubiquitous and functionally critical component of terrestrial ecosystems. In this paper, we utilize a biogeography database summarizing data on AMF species distribution linked to geographic and environmental conditions to describe global distribution patterns and interpret these patterns within a phylogenetic perspective. The data were obtained from accessions in living culture collections (INVAM, CICG), species descriptions, and other published literature from 1960 to 2012. The database contains 7105 records, 6396 of them from 768 published papers and the remaining 709 from culture accessions. Glomeromycotan species were recorded in all seven continents, 87 countries, 11 biogeographical realms, and 14 biomes. The distribution of families differed among climatic zones and continents, but they, together with all genera, appear to be cosmopolitan. Distribution of AMF species shows a slight decrease from low to high latitudes, but this decrease is steeper in the southern than in the northern hemisphere. A total of 189 species is shared between ancient supercontinents Gondwana and Laurasia and 78 species are common to all climatic zones. Ninety-five species (43% of the total) have known cosmopolitan distribution, including members of all genera except Redeckera. Some species have disjunct distribution and 26% of species have been registered from only one continent. Data on AMF distribution challenge the “Everything is everywhere” hypothesis in favor of the “moderate endemicity model” for species distribution. Data from this study provide a foundation to formulate and test hypotheses of biogeographic patterns and processes in Glomeromycota.

Keywords

Ancient continents Climatic zones EiE hypothesis Moderate endemicity model Patterns of distribution Species distribution 

Notes

Acknowledgments

SLS thanks the Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq) Brazil for a Research Assistantship (Process 309.163/2015-3) and Universidade Regional de Blumenau (FURB) for supporting a sabbatical leave at the University of Kansas. JDB thanks the U.S. National Science Foundation (grant 1556664) for funding. JBM thanks the U.S. National Science Foundation (grant DBI0650735) for funding. We are indebted to Paolo Moser for guidance in statistical analysis. We thank Karl Kemmelmeier, Camille Delavaux, and Robert Ramos for suggestions and discussion of the manuscript. We are indebted to Caroline Krug Vieira for editing Table S1.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

572_2018_864_MOESM1_ESM.xlsx (716 kb)
ESM 1 (XLSX 715 kb)
572_2018_864_MOESM2_ESM.pdf (629 kb)
ESM 2 (PDF 628 kb)
572_2018_864_MOESM3_ESM.pdf (185 kb)
ESM 3 (PDF 184 kb)
572_2018_864_MOESM4_ESM.pdf (424 kb)
ESM 4 (PDF 423 kb)
572_2018_864_MOESM5_ESM.pdf (245 kb)
ESM 5 (PDF 245 kb)
572_2018_864_MOESM6_ESM.pdf (434 kb)
ESM 6 (PDF 434 kb)
572_2018_864_MOESM7_ESM.pdf (675 kb)
ESM 7 (PDF 675 kb)

References

  1. Allen MF, Hipps LE, Woolridge GL (1989) Wind dispersal and subsequent establishment of VA mycorrhizal fungi across a successional arid landscape. Landsc Ecol 2:165–171CrossRefGoogle Scholar
  2. Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. In: Collins HP, Robertson GP, Klug MJ (eds) The significance and regulation of soil biodiversity. Kluwer Academic Publishers, NetherlandsGoogle Scholar
  3. Blaszkowski J, Chwat G (2013) Septoglomus deserticola emended and new combinations in the emended definition of the family Diversisporaceae. Acta Mycol 48:89–103CrossRefGoogle Scholar
  4. Brown JH, Lomolino MV (1998) Biogeography. 2nd Edn. Sinauer Associates, Inc. Publishers. Sunderland, Massachusetts p 691Google Scholar
  5. Brown JH, Lomolino MV (2008) Biogeography, 2nd edn. Sinauer Associates, Inc. Publishers, Sunderland p 691Google Scholar
  6. Brundrett MC (1991) Mycorrhizas in natural ecosystems. Adv Ecol Res 21:171–213CrossRefGoogle Scholar
  7. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol.  https://doi.org/10.1111/nph.14976
  8. Bruns TD, Taylor JW (2016) Comment on “Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism”. Science 351:826CrossRefGoogle Scholar
  9. Carr M, Baldauf SL (2011) The protistan origins of animals and fungi. In: Pöggeler S, Wöstemeyer (eds) Evolution of fungi and fungal-like organisms, The Mycota XIV. Springer-Verlag, BerlinGoogle Scholar
  10. Chaudhary VB, Lau MK, Johnson NC (2008) Macroecology of microbes—biogeography of the Glomeromycota. In: Varma A (ed) Mycorrhiza. Springer-Verlag, BerlinGoogle Scholar
  11. Chaudhary VB, Cuenca G, Johnson NC (2018) Tropical-temperate comparison of landscape-scale arbuscular mycorrhizal fungal species distributions. Divers Distrib 24:116–128CrossRefGoogle Scholar
  12. Cox CB, Moore PD (2010) Biogeography—an ecological and evolutionary approach. John Wiley & Sons, Inc., USAGoogle Scholar
  13. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Bdiaye C, Pärtel M, Reier U, Saks U, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973CrossRefGoogle Scholar
  14. Diem HG, Gueye I, Gianinazzi-Pearson V, Fortin JA, Dommergues YR (1981) Ecology of VA mycorrhizae in the tropics: the semi-arid zone of Senegal. Acta Oecol 2:53–62Google Scholar
  15. Dotzler N, Krings M, Taylor TN, Agerer R (2006) Germination shields in Scutellospora (Glomeromycota: Diversisporales, Gigasporaceae) from the 400 million-year-old Rhynie chert. Mycol Prog 5:178–184CrossRefGoogle Scholar
  16. Dotzler N, Walker C, Krings M, Hass H, Kerp H, Taylor TN, Agerer R (2009) Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert. Mycol Prog 8:9–18CrossRefGoogle Scholar
  17. Eom AH, Hartnett DC, Wilson GWT (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122:435–444CrossRefGoogle Scholar
  18. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc. Natl Acad Sci U S A 103:626–631CrossRefGoogle Scholar
  19. Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45:111–136Google Scholar
  20. Foissner W (2008) Protist diversity and distribution: some basic considerations. Biodivers Conserv 17:235–242CrossRefGoogle Scholar
  21. Fracchia S, Krapovickas L, Aranda-Rickert A, Valentinuzzi VS (2011) Dispersal of arbuscular mycorrhizal fungi and dark septate endophytes by Ctenomys cf. knighti (Rodentia) in the northern Monte Desert of Argentina. J Arid Environ 75:1016–1023CrossRefGoogle Scholar
  22. Friese CF, Allen MF (1993) The interaction of harvester ants and vesicular-arbuscular mycorrhizal fungi in a patchy semiarid environment—the effects of mound structure on fungal dispersion and establishment. Funct Ecol 7:13–20CrossRefGoogle Scholar
  23. Gianinazzi-Pearson V, Diem HG (1982) Endomycorrhizae in the tropics. In: Dommergues YE, Diem HG (eds) Microbiology of tropical soils and plant productivity. Martinus Nijhoff, Le HavreGoogle Scholar
  24. Hawkins BA, Porter EE, Felizola Diniz-Filho JA (2003) Productivity and history as predictors of the latitudinal diversity gradient of terrestrial birds. Ecology 84:1608–1623CrossRefGoogle Scholar
  25. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133CrossRefGoogle Scholar
  26. Herrera RA, Ferrer EL (1980) Vesicular-arbuscular mycorrhiza in Cuba. In: Mikola P (ed) Tropical mycorrhiza research. Clarendon Press, OxfordGoogle Scholar
  27. Holt BG, Lessard J-P, Borregaard MK, Fritz SA, Araújo MB, Dimitrov D, Fabre P-H, Graham CH, Graves GR, Jønsson KA, Nogués-Bravo D, Wang Z, Whittaker RJ, Fjeldså J, Rahbek C (2013) An update of Wallace’s zoogeographical regions of the world. Science 339:74–78 Reprinted with permission from AAASCrossRefGoogle Scholar
  28. House GL, Ekanayake S, Ruan Y, Schutte UME, Kaonongbua W, Fox G, Ye Y, Bever JD (2016) Phylogenetic structured differences in rRNA gene sequence variation among species of arbuscular mycorrhizal fungi and their implications for sequence clustering. Appl Environ Microbiol 82:4921–4930CrossRefGoogle Scholar
  29. Jabiol J, Bruder A, Gessner MO, Makkonen M, Mckie BG, Peeters ETHM, Vos VCA, Chauvet E (2013) Diversity patterns of leaf-associated aquatic hyphomycetes along a broad latitudinal gradiente. Fungal Ecol 6:439–448CrossRefGoogle Scholar
  30. Janos DP, Sahley CT, Emmons LH (1995) Rodent dispersal of vesicular-arbuscular mycorrhizal fungi in Amazonian Peru. Ecology 76:1852–1858CrossRefGoogle Scholar
  31. Ji B, Bentivenga JP, Casper BB (2012) Comparisons of AM fungal spore communities with the same hosts but different soil chemistries over local and geographical scales. Oecologia 168:187–197CrossRefGoogle Scholar
  32. Johnson D, van der Koornhusye PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grasslands microcosms. New Phytol 161:502–515Google Scholar
  33. Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303CrossRefGoogle Scholar
  34. Koske RE (1987) Distribution of VA mycorrhizal fungi along a latitudinal temperature gradient. Mycologia 79:55–68CrossRefGoogle Scholar
  35. Koske RE, Gemma JN (1990) VA-mycorrhizae in strand vegetation of Hawaii—evidence for long-distance codispersal of plants and fungi. Am J Bot 77:466–474CrossRefGoogle Scholar
  36. Koske RE, Gemma JN (1995) Scutellospora hawaiiensis: a new species of arbuscular mycorrhizal fungus from Hawaii. Mycologia 87:678–683CrossRefGoogle Scholar
  37. Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2011) 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
  38. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam p 853Google Scholar
  39. Linzey DW (2012) Vertebrate biology. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  40. Lovelock CE, Andersen K, Morton JB (2003) Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia 135:268–279CrossRefGoogle Scholar
  41. Mangan SA, Adler GH (2000) Consumption of arbuscular mycorrhizal fungi by terrestrial and arboreal small mammals in a Panamanian cloud forest. J Mammal 81:563–570CrossRefGoogle Scholar
  42. Mello CMA, Silva GA, Assis DMA, Pontes JS, Ferreira ACA, Leão MPC, Vieira HEE, Maia LC, Oehl F (2013) Paraglomus pernambucanum sp. nov. and Paraglomus bolivianum comb. nov., and biogeographic distribution of Paraglomus and Pacispora. J Appl Bot Food Qual 86:113–125Google Scholar
  43. Mendez A (2011) Distribution of landmasses of the Paleo-Earth. Planetary Habitability Laboratory. http://phl.upr.edu/library/notes/distributionoflandmassesofthepaleo-earth. Accessed 14 Nov 2014
  44. Morton JB (1993) Problems and solution for the integration of glomalean taxonomy, systematic biology, and the study of mycorrhizal phenomena. Mycorrhiza 2:97–109CrossRefGoogle Scholar
  45. Morton JB, Redecker D (2001) Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93:181–195CrossRefGoogle Scholar
  46. Morton JB, Bentivenga SP, Bever JD (1995) Discovery, measurement, and interpretation of diversity in arbuscular endomycorrhizal fungi (Glomales, Zygomycetes). Can J Bot 73(suppl. 1):S25–S32CrossRefGoogle Scholar
  47. Oehl F, Silva GA, Palenzuela J, Sánchez-Castro I, Castillo C, Sieverding E (2011) Acaulospora punctata, a new fungal species in the glomeromycetes from mountainous altitudes of the Swiss Alps and Chilean Andes. Nova Hedwigia 93:353–362CrossRefGoogle Scholar
  48. Olson DM, Dinerstein E, Wikramanayake ED, Burges ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51:933–938CrossRefGoogle Scholar
  49. Öpik M, Vanatoa A, Vanatoa E, Mora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribuition patterns in arbuscular mycorrhizla fungi (Glomeromycota). New Phytol 188:223–241CrossRefGoogle Scholar
  50. 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 23:411–430CrossRefGoogle Scholar
  51. Parenti LR, Ebach MC (2009) Comparative biogeography—discovering and classifying biogeographical patterns of a dynamic earth. Univ of California Press, Berkeley p 291Google Scholar
  52. Pärtel M, Öpik M, Moora M, Tedersoo L, Szava-Kovats R, Rosendahl S, Rillig MC, Lekberg Y, Kreft H, Helgason T, Eriksson O, Davison J, Bello F, Caruso T, Zobel M (2017) Historical biome distribution and recent human disturbance shape the diversity of arbuscular mycorrhizal fungi. New Phytol 216:227–238CrossRefGoogle Scholar
  53. Powell JR, Benett AE (2016) Unpredictable assembly of arbuscular mycorrhizal fungal communities. Pedobiologia 59:11–15CrossRefGoogle Scholar
  54. Qian H (1999) Spatial patterns of vascular plant diversity in North America North of Mexico and its floristic relationship with Eurasia. Ann Bot 83:271–283CrossRefGoogle Scholar
  55. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492CrossRefGoogle Scholar
  56. Redecker D, Kodner R, Graham LE (2002) Palaeoglomus grayi from the Ordovician. Mycotaxon 84:33–37Google Scholar
  57. Redecker D, Schussler A, Stockinger H, Sturmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531CrossRefGoogle Scholar
  58. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci 91:11841–11843CrossRefGoogle Scholar
  59. Rosendahl S, McGee P, Morton JB (2009) Lack of global population genetic differentiation in the arbuscular mycorrhizal fungi Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 18:4316–4329CrossRefGoogle Scholar
  60. Rosenzweig ML (1995) Species diversity in space and time. Cambridge University, CambridgeCrossRefGoogle Scholar
  61. Savary R, Masclaux FG, Wyss T, Droh G, Corella JC, Machado AP, Morton JB, Sanders IR (2018) A population genomics approach shows widespread geographical distribution of cryptic genomic forms of the symbiotic fungus Rhizophagus irregularis. ISME J 12:17–30CrossRefGoogle Scholar
  62. Schenck NC, Graham SO, Green NE (1975) Temperature and light effect on contamination and spore germination of vesicular-arbuscular mycorrhizal fungi. Mycologia 67:1189–1192CrossRefGoogle Scholar
  63. Scotese CE (2004) A continental drift flipbook. J Geol 112:729–741CrossRefGoogle Scholar
  64. Simon L, Bousquet R, Levesque RC, Lalone M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69CrossRefGoogle Scholar
  65. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, LondonGoogle Scholar
  66. Stürmer SL, Bellei MM (1994) Composition and seasonal variation of spore populations of arbuscular mycorrhizal fungi in dune soils on the island of Santa Catarina. Brazil Can J Bot 72:359–363CrossRefGoogle Scholar
  67. Stürmer SL, Oliveira LZ, Morton JB (2018) Gigasporaceae versus Glomeraceae (phylum Glomeromycota): a biogeographic tale of dominance in maritime sand dunes. Fungal Ecol 32:49–56CrossRefGoogle Scholar
  68. Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia 87:560–573CrossRefGoogle Scholar
  69. Tedersoo L (2017) Biogeography of mycorrhizal symbiosis. Springer International Publishing, SwitzerlandCrossRefGoogle Scholar
  70. Tedersoo L, Nara K (2010) General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol 185:351–354CrossRefGoogle Scholar
  71. Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Poldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Partel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson KH, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, de Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346(6213):1256688CrossRefGoogle Scholar
  72. Trappe J (1987) Phylogenetic and ecological aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir G (ed) Ecophysiology of VA mycorrhizal plants. CRC Press, Boca Raton, FloridaGoogle Scholar
  73. 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 22:81–97CrossRefGoogle Scholar
  74. Walker C (1992) Systematics and taxonomy of the arbuscular mycorrhizal fungi (Glomales)—a possible way forward. Agronomie 12:887–897CrossRefGoogle Scholar
  75. Walker C, Gollotte A, Redecker D (2018) A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis). Mycorrhiza 28:213–219.  https://doi.org/10.1007/s00572-017-0815-7 CrossRefPubMedGoogle Scholar
  76. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefGoogle Scholar
  77. Williams DM (2011) Historical biogeography, microbial endemism and the role of classification: everything is endemic. In: Fontaneto D (ed) Biogeography of microscopic organisms—is everything small everywhere? Cambridge University Press, CambridgeGoogle Scholar
  78. Yang H, Dai Y, Xu M, Zhang Q, Bian X, Tang J, Chen X (2016) Metadata-mining of 18S rDNA sequences reveals that “everything is not everywhere” for glomeromycotan fungi. Ann Microbiol 66:361–371CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departamento de Ciências NaturaisUniversidade Regional de BlumenauBlumenauBrazil
  2. 2.Department of Ecology and Evolutionary Biology and Kansas Biological SurveyThe University of KansasLawrenceUSA
  3. 3.West Virginia UniversityMorgantownUSA

Personalised recommendations