Skip to main content
Log in

Metadata-mining of 18S rDNA sequences reveals that “everything is not everywhere” for glomeromycotan fungi

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

In microbial ecology, the “everything is everywhere” hypothesis has long been controversial. In the present study, we performed data-mining for 18S rDNA sequences of glomeromycotan fungi in order to test this hypothesis. 18S rDNA sequences targeted using AM1–NS31 fragments were retrieved from GenBank, with a total of 1768 sequences collected from 34 sites worldwide. In total, 229, 330 and 518 operational taxonomic units (OTUs) were defined based on 97, 98 and 99 % similarity, respectively. The 97 % OTUs showed a limited geographical range of glomeromycotan fungi. Among the OTUs, 58.1 % were endemic, and 17.9 % and 9.2 % were found in two and three sites, respectively. The most widespread OTU was shared by 17 sites. Phylogenetic structure analysis demonstrated that most local communities (26 of 34) were clustered. OTUs with larger host breadth had wider geographic ranges. A significant distance–decay relationship was revealed that was independent of habitat. Cluster analysis showed that fungal composition was not related to habitat, while Fast UniFrac analysis indicated that the distribution of Glomeromycota was affected by temperature. Taken together, these results suggest that glomeromycotan fungi were not randomly distributed under natural conditions; rather, they were affected by host plants, dispersal ability and temperature. Thus, the distribution of glomeromycotan fungi argues against the hypothesis that “everything is everywhere.”

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Baar J, Paradi I, Lucassen ECHET, Hudson-Edwards KA, Redecker D, Roelofs JGM, Smolders AJP (2011) Molecular analysis of AMF diversity in aquatic macrophytes: a comparison of oligotrophic and utra-oligotrophic lakes. Aquat Bot 94:53–61

    Article  CAS  Google Scholar 

  • Bell T, Ager D, Song JI, Newman JA, Thompson IP, Lilley AK, Van Der Gast CJ (2005) Larger islands house more bacterial taxa. Science 308:1884

    Article  CAS  PubMed  Google Scholar 

  • Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominguez L, Sersic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392

    Article  CAS  PubMed  Google Scholar 

  • Chaudhary V, Lau M & Johnson N (2008) Macroecology of microbes – biogeography of the Glomeromycota. In: Varma A ed. Mycorrhiza: Springer Berlin Heidelberg, 529–563

  • Darling KF, Wade CM, Stewart IA, Kroon D, Dingle R, Brown AJL (2000) Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405:43–47

    Article  CAS  PubMed  Google Scholar 

  • Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255

    Article  Google Scholar 

  • Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T & Wilson A (2010) Geneious v5.1, Available from http://www.geneious.com

  • Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

    Article  Google Scholar 

  • Finlay BJ, Esteban GF, Olmo JL, Tyler PA (1999) Global distribution of free-living microbial species. Ecography 22:138–144

    Article  Google Scholar 

  • Fiz-Palacios O, Schneider H, Heinrichs J, Savolainen V (2011) Diversification of land plants: insights from a family-level phylogenetic analysis. BMC Evol Biol 11:341

    Article  PubMed Central  PubMed  Google Scholar 

  • Gai JP, Christie P, Cai XB, Fan JQ, Zhang JL, Feng G, Li XL (2009) Occurrence and distribution of arbuscular mycorrhizal fungal species in three types of grassland community of the Tibetan Plateau. Ecol Res 24:1345–1350

    Article  Google Scholar 

  • Glockner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66:5053

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gosling P, Mead A, Proctor M, Hammond JP, Bending GD (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M, Gillings M, Beattie AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750

    Article  CAS  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT & Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Available at http://folk.uio.no/ohammer/past/. Accessed May 20, 2009

  • Heinemeyer A, Ridgway KP, Edwards EJ, Benham DG, Young JPW, Fitter AH (2004) Impact of soil warming and shading on colonization and community structure of arbuscular mycorrhizal fungi in roots of a native grassland community. Glob Chang Biol 10:52–64

    Article  Google Scholar 

  • Heino J, Bini LM, Karjalainen SM, Mykra H, Soininen J, Vieira LCG, Diniz JAF (2010) Geographical patterns of micro-organismal community structure: are diatoms ubiquitously distributed across boreal streams? Oikos 119:129–137

    Article  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431

    Article  CAS  PubMed  Google Scholar 

  • Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384

    Article  Google Scholar 

  • Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM (2004) A taxa - area relationship for bacteria. Nature 432:750–753

    Article  CAS  PubMed  Google Scholar 

  • Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678

    Article  CAS  PubMed  Google Scholar 

  • Koske R (1987) Distribution of VA mycorrhizal fungi along a latitudinal temperature gradient. Mycologia 79:55–68

    Article  Google Scholar 

  • Kottek M, Grieser J, Beck C, Bruno R, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263

    Article  Google Scholar 

  • Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105

    Article  Google Scholar 

  • Li LF, Li T, Zhang Y, Zhao ZW (2010a) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, southwest China. FEMS Microbiol Ecol 71:418–427

    Article  CAS  PubMed  Google Scholar 

  • Li T, Li L, Sha T, Zhang H, Zhao Z (2010b) Molecular diversity of arbuscular mycorrhizal fungi associated with two dominant xerophytes in a valley-type savanna, southwest China. Appl Soil Ecol 44:61–66

    Article  Google Scholar 

  • Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG (2007) Glomeromycotean associations in liverworts: a molecular cellular and taxonomic analysis. Am J Bot 94:1756–1777

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Shi G, Mao L, Cheng G, Jiang S, Ma X, An L, Du G, Collins Johnson N, Feng H (2012) Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523–535

    Article  CAS  PubMed  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lozupone C, Hamady M, Knight R (2006) UniFrac - An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinf 7:371

    Article  Google Scholar 

  • 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 55:705–713

    Article  CAS  PubMed  Google Scholar 

  • Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  PubMed  Google Scholar 

  • Noguez AM, Arita HT, Escalante AE, Forney LJ, Garcia-Oliva F, Souza V (2005) Microbial macroecology: highly structured prokaryotic soil assemblages in a tropical deciduous forest. Glob Ecol Biogeogr 14:241–248

    Article  Google Scholar 

  • Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179:867–876

    Article  PubMed  Google Scholar 

  • Pietikainen A, Kytoviita M-M, Husband R, Young JPW (2007) Diversity and persistence of arbuscular mycorrhizas in a low-Arctic meadow habitat. New Phytol 176:691–698

    Article  CAS  PubMed  Google Scholar 

  • Pirozynski KA, Malloch DW (1975) The origin of land plants: a matter of mycotrophism. Biosystems 6:153–164

    Article  CAS  PubMed  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  CAS  PubMed  Google Scholar 

  • Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, Bothe H (2003) Colonization of pennycresses (Thlaspi spp.) of the Brassicaceae by arbuscular mycorrhizal fungi. J Plant Physiol 160:615–626

    Article  CAS  PubMed  Google Scholar 

  • Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266

    Article  PubMed  Google Scholar 

  • Rosendahl S, Mcgee P, Morton JB (2009) Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 18:4316–4329

    Article  PubMed  Google Scholar 

  • Russell J, Bulman S (2005) The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol 165:567–579

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scotese C (2004) A continental drift flipbook. J Geol 112:729–741

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic press, Inc, San Diego

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Steenkamp ET, Stepkowski T, Przymusiak A, Botha WJ, Law IJ (2008) Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harboring nodulation genes that belong to the large pantropical clade common in Africa. Mol Phylogenet Evol 48:1131–1144

    Article  CAS  PubMed  Google Scholar 

  • Usher KM, Fromont J, Sutton DC, Toze S (2004) The Biogeography and phylogeny of unicellular cyanobacterial symbionts in sponges from Australia and the Mediterranean. Microb Ecol 48:167–177

    Article  CAS  PubMed  Google Scholar 

  • Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JP (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564

    Article  CAS  PubMed  Google Scholar 

  • Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Yeun LH, Xue JY, Liu Y, Ane JM, Qiu YL (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525

    Article  PubMed  Google Scholar 

  • Wang Y, Huang Y, Qiu Q, Xin G, Yang Z, Shi S (2011) Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS One 6:e24512

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155

    Article  PubMed  Google Scholar 

  • West B, Brandt J, Holstien K, Hill A, Hill M (2009) Fern-associated arbuscular mycorrhizal fungi are represented by multiple Glomus spp.: do environmental factors influence partner identity? Mycorrhiza 19:295–304

    Article  PubMed  Google Scholar 

  • Wilde P, Manal A, Stodden M, Sieverding E, Hildebrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11:1548–1561

    Article  PubMed  Google Scholar 

  • Wirtz N, Printzen C, Lumbsch HT (2008) The delimitation of Antarctic and bipolar species of neuropogonoid Usnea (Ascomycota, Lecanorales): a cohesion approach of species recognition for the Usnea perpusilla complex. Mycol Res 112:472–484

  • Wu BY, Hogetsu T, Isobe K, Ishii R (2007) Community structure of arbuscular mycorrhizal fungi in a primary successional volcanic desert on the southeast slope of Mount Fuji. Mycorrhiza 17:495–506

    Article  CAS  PubMed  Google Scholar 

  • Wubet T, Weiss M, Kottke I, Teketay D, Oberwinkler F (2006) Phylogenetic analysis of nuclear small subunit rDNA sequences suggests that the endangered African Pencil Cedar, Juniperus procera, is associated with distinct members of Glomeraceae. Mycol Res 110:1059–1069

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Zang Y, Yuan Y, Tang J, Chen X (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:50

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the National Natural Science Foundation of China (No.31400373), Natural Science Foundation of Jiangsu Province (No.BK20140689) and China Postdoctoral Science Foundation (No.2014 M561659), and the Fundamental Research Funds for the Central Universities (No.KJQN201502). We also thank Dr. Jean W.H. Yong for comments in the manuscript revision.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Haishui Yang or Xin Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(GIF 15 kb)

High-resolution image (TIFF 712 kb)

ESM 2

(PDF 53 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, H., Dai, Y., Xu, M. et al. Metadata-mining of 18S rDNA sequences reveals that “everything is not everywhere” for glomeromycotan fungi. Ann Microbiol 66, 361–371 (2016). https://doi.org/10.1007/s13213-015-1116-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-015-1116-z

Keywords

Navigation