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Keywords:

  • distribution;
  • diversity;
  • geographical range;
  • habitat;
  • rDNA;
  • soil communities;
  • soil fungi

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  • 1
    Arbuscular mycorrhizal (AM) fungi are obligate root symbionts that are present in most terrestrial ecosystems and have roles in plant mineral nutrition, carbon cycling and biotic interactions. In this work, 26 publications were surveyed that report on the occurrence of natural root-colonizing AM fungi identified using rDNA region sequences. A total of 52 host plant species were investigated. Sixteen publications provided data enabling a comparison to be made of AM fungal taxon richness and community composition across 36 host plant species and 25 locations. Ninety-five fungal taxa (small subunit rRNA gene sequence types) were involved, 49 of which were recorded from at least two study sites, and 65 from more than one host plant species.
  • 2
    The number of AM fungal taxa per host plant species differed between habitat types: a significantly higher richness was found in tropical forests (18.2 fungal taxa per plant species), followed by grasslands (8.3), temperate forests (5.6) and habitats under anthropogenic influence (arable fields and polluted sites, 5.2).
  • 3
    AM fungal communities exhibit differing compositions in broadly defined habitat types: tropical forests, temperate forests and habitats under anthropogenic influence. Grassland locations around the world host heterogeneous AM fungal communities.
  • 4
    A number of AM fungi had a global distribution, including sequence types related to the Glomus intraradices/fasciculatum group, G. mosseae, G. sp. UY1225 and G. hoi, as well as the Glomus and Scutellospora types of unknown taxonomic affiliation. Widespread taxa occur in both natural and anthropogenic (disturbed) habitats, and may show high local abundance. However, about 50% of taxa have been recorded from only a single site.
  • 5
    The current global analysis of AM fungal communities suggests that soil micro-organisms may exhibit different distribution patterns, resulting in a high variability of taxon richness and composition between particular ecosystems.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Ecology has long studied the distribution of species assemblages along environmental gradients. Regional descriptions are usually focused on the species composition and physiognomy of vascular plant communities (e.g. Ellenberg et al. 1991; Rodwell 1991). There is, however, also extensive information about the large-scale variation of the biological diversity of other taxonomic groups (Gaston 2000; Rosenzweig 2000). Although micro-organisms comprise much of the Earth's biodiversity and have critically important roles in ecosystem functioning, little is known about their spatial diversification (Fitter 2005). Recent evidence has shown that microbes can exhibit a taxa–area relationship (Horner-Devine et al. 2004), and suggests that despite high local diversity, micro-organisms may have only moderate regional diversity (Green et al. 2004). More effort is, however, needed in order to establish general patterns of variation in microbial diversity.

Arbuscular mycorrhizal (AM) fungi (phylum Glomeromycota) are thought to be the oldest group of organisms living in symbiosis with land plants (Blackwell 2000; Redecker et al. 2000). More than 150 species have been described (Schüßler et al. 2001), primarily on the basis of spore morphology. AM fungi colonize the roots of most land plants, where they facilitate mineral nutrient uptake from the soil in exchange for plant-assimilated carbon (Smith & Read 1997). In recent years, more information has been gathered regarding the functional role of AM fungi in ecosystems (van der Heijden & Sanders 2002). In particular, there is evidence that experimental (van der Heijden et al. 1998a,b) and natural (Moora et al. 2004) AM fungal communities with different taxon composition may induce a different growth response in plants, and may thus influence the structure and composition of vascular plant communities. In order to understand factors structuring plant communities, more information is needed about the natural distribution patterns of AM fungi. However, owing to the soil-borne nature, uncultivability and limited means for the identification of AM fungi, ‘descriptive data on their community structure in different environments is sadly lacking’ (Sanders 2004).

In order to generalize the variation in the diversity and composition of AM fungal communities in different environments, we present an overview of currently available surveys of AM fungal taxa detected in various plant communities worldwide. We focus on AM fungal communities inside plant roots, which are considered to comprise the symbiotically active fungi. The analysis of spore communities in soil is beyond the scope of the present paper.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

surveyed publications

Twenty-six publications were surveyed (Table 1) that describe AM fungal communities in the roots of plants growing in natural conditions or on natural soil in experimental conditions (glasshouse experiment – part of the data in Öpik et al. 2003; sowed experimental grassland –Heinemeyer et al. 2004; field experiment –Jumpponen et al. 2005).

Table 1.  Overview of arbuscular mycorrhizal (AM) fungal community surveys from different ecosystems in relation to sampling and sample screening. Sixteen publications used for comparative community analyses are highlighted in bold type and consecutively numbered; study sites are coded with letters (e.g. site b of ref. 2 is the same as site b in ref. 3) as in Fig. 2
EcosystemReferenceRef. and site codeNo. of sitesPlant speciesNo. of root samplesNo. of clones screenedNo. of clones sequencedNo. of AMF taxa per siteTotal no. of AMF taxaDiversity indexMarker regionPrimers used
Forests
Afromontane: Ethiopia Wubet et al. (2004)   2 Prunus africana (Rosaceae)50  92 9211/15202.58ITSFamily specific, nested PCR
Boreal (Scots pine): Estonia Öpik et al. (2003) 1a  1 Pulsatilla patens, P. pratensis (Ranunculaceae)26 202 831010 SSUNS31–AM1
Coniferous (spruce + yew): GermanyWubet et al. (2003)  1 Taxus baccata (Taxaceae) 5? 16 2 2 ITSFamily specific, nested PCR
Montane cloud forest: Ecuador Haug et al. (2004)1  Graffenrieda emarginata (Melastomataceae) 4? 13 6 6 ITS, SSUFamily specific, nested PCR
Seminatural broadleaved forest: UK, Yorkshire Helgason et al. (1998)   1 Ajuga reptans, Glechoma hederacea (Lamiaceae), Epilobium angustifolium (Onagraceae), Hyacinthoides non-scripta (Liliaceae), Rubus fruticosus (Rosaceae) ? 154 2211111.44SSUNS31–AM1
Helgason et al. (1999 ) 2b  1 Hyacinthoides non-scripta 16/17 141 62 7/8 91.36–1.62SSUNS31–AM1
Tropical rainforest: Panama Helgason et al. (2002 ) 3b  1 Acer pseudoplatanus (Aceraceae), Ajuga reptans, Epilobium angustifolium, Glechoma hederacea, Rubus fruticosus22/15 116 60 8/611 SSUNS31–AM1
Husband et al. (2002b ) 4c  1 Tetragastris panamensis (Burseraceae)20 558 1018180.79–1.96SSUNS31–AM1
Husband et al. (2002a) 5d,e,f  3 Faramea occidentalis (Rubiaceae), Luehea seemannii (Tiliaceae), Tetragastris panamensis541536 9018/18/22292.33SSUNS31–AM1
Temperate grasslands
Dune grassland: Netherlands Scheublin et al. (2004) 6g  1 Festuca ovina (Poaceae), Hieracium pilosella (Compositae), Plantago lanceolata (Plantaginaceae), Lotus corniculatus, Ononis repens, Trifolium repens (Leguminosae)25562 4715151.77SSUNS31–AM1
Coastal grassland: DenmarkRosendahl & Stukenbrock (2004)  1 Hieracium pilosella (Compositae)???1010 LSU Glomus-specific, nested PCR
Experimental grassland: UK Heinemeyer et al. (2004) 7h  1Pooled roots’ sample (Agrostis capillaris, Cynosurus cristatus, Festuca rubra, Holcus lanatus (Poaceae), Plantago lanceolata, Trifolium repens)45509 191010 SSUNS31–AM1
Temperate grassland: Estonia Öpik et al. (2003 ) 1i,j  2 Pulsatilla patens, P. pratensis (Ranunculaceae)24158 431414 SSUNS31–AM1
France Vandenkoornhuyse et al. (2002a) 8k  1 Arrhenaterium elatius (Poaceae)> 3200200 3 3 SSUGeneral fungal
Japan Saito et al. (2004) 9L,m  2 Miscanthus sinensis, Zoysia japonica (Poaceae)24/24247 + 892 6419/1624 SSUGlomeromycota- specific, nested PCR
Upland grassland: UK, Scottish Borders Gollotte et al. (2005)   1 Agrostis capillaris, Lolium perenne (Poaceae)2 (pooled from 36)100 601010 LSUGroup-specific, nested PCr
Vandenkoornhuyse et al. (2002b) 10n  1 Agrostis capillaris, Trifolium repens35/121494/507 8821211.71SSUNS31–AM1
Prairie: USA, Kansas Jumpponen et al. (2005) 11o  1Pooled roots’ sample (Andropogon gerardii, Panicum virgatum, Sorghastrum nutans; Poaceae)4 (pooled from 24)200 371010 SSUNS31–AM1
Oak woodland/grassland: USA, California Douhan et al. (2005) 12p  1 Cynosurus echinatus (Poaceae), Torilis arvensis (Apiaceae), Quercus douglasii (Fagaceae)14/2/179 57 8 8 SSUNS31–AM1
Arable fields
Denmark Kjøller & Rosendahl (2001)   1 Pisum sativum (Leguminosae)95SSCP39 SSCP 4 4 LSU Glomus-specific, nested PCR
UK Daniell et al. (2001) 13r,s,t  3 Hordeum vulgare, Triticum aestivum, Zea mays (Poaceae), Pisum sativum17/39/15/8303 727/7/3100.45–1.49SSUNS31–AM1
Helgason et al. (1998)  3 Pisum sativum, Triticum aestivum, Zea mays?100  81/3/4 70.40SSUNS31–AM1
Other
Aquatic plants in oligotrophic lakes: Sweden Nielsen et al. (2004)   6 Littorella uniflora (Plantaginaceae), Lobelia dortmanna (Campanulaceae)117154 SSCP29 (bands)4/4/4/5/5/6 8 LSUGroup-specific, nested PCR
Cultivated site: Germany Wubet et al. (2003)   1 Taxus baccata (Taxaceae)5? 16 3 3 ITSFamily specific, nested PCR
Epiparasitic plants in subantarctic forest: Argentina Bidartondo et al. (2002)  3 Arachnitis uniflora (Corsiaceae)8??1/1/1 1 ITS, SSUGeneral fungal ITS1F–ITS4
French Guyana Bidartondo et al. (2002)  2 Voyriella parviflora, Voyria rosea, V. tenuiflora, V. corymbosa, V. caerulea, V. aurantiaca (Gentianaceae)12??3/2 4 ITS, SSUFamily specific, nested PCR
Heavy metal polluted soils: UK Whitfield et al. (2004) 14u,v,w  3 Thymus polytrichus (Lamiaceae)3/3/2 60166/4/6 9 SSUNS31–AM1
Liverworts: New Zealand Russell & Bulman (2005)  10 Marchantia foliacea (Marchantiales)10??1 4 ITS, SSUVarious, nested PCR
Temperate wetland: Germany Wirsel (2004) 15x,y  2 Phragmites australis (Poaceae)6/75465412/16162.4SSUNS31–AM1; ITS4–ARCH1311
Area affected by lahars (mud flows): Philippines Oba et al. (2004) 16z  2 Saccharum spontaneum, Rhynchelytrum repens (Poaceae), Calpogonium mucunoides (Leguminosae)4 53535/6 7 SSUNS31–AM1

AM fungal community composition data from 16 studies (marked bold type in Table 1) using the comparable SSU rRNA gene region were analysed in more detail. Data from these publications were compiled into a host plant- (at study site) based matrix, including 52 plant species from 25 sites and 95 AM fungal sequence types. Only data concerning autotrophic higher plants were used. One study, presumably presenting data that overlap with a later publication (Helgason et al. 1998), was not included. Host plants represented by only one sample were also not included: Quercus douglasii (Douhan et al. 2005), Rhynchelytrum repens and Saccharum spontaneum (Oba et al. 2004), and few locations of Pulsatilla spp. (Öpik et al. 2003); unique AM fungi have not been detected in such samples. Most of the surveyed studies had utilized the primer pair NS31–AM1 covering a c. 500-bp central fragment of the SSU rRNA gene. The primer pair is known to amplify most taxa of the Glomeromycota, but to exclude the basal families Archaeosporaceae and Paraglomaceae (Daniell et al. 2001). In some cases, other primers had been exploited: Saito et al. (2004) used newly designed primers presumably amplifying all Glomeromycota; Wirsel (2004) applied both NS31–AM1 and primers amplifying the basal families; and Vandenkoornhuyse et al. (2002a) used general fungal primers. Representatives of all AM fungal sequence types were subjected to a BLAST search (Altschul et al. 1997) in order to identify synonymous groups at a similarity level of 97–98%. In some cases, groups originally distinguished by the authors were merged.

AM fungi have been identified in the above studies as sequence types or genotypes, based on phylogenetic analysis and the grouping of related root-derived fungal sequences. Conceding the problems involved in relating these groupings to fungal species (e.g. see Sanders 2004; van der Heijden et al. 2004), we refer to them as ‘taxa’, and avoid the use of the term ‘species’.

data analysis

In order to analyse the variation in AM fungal taxon richness (the number of fungal taxa in a sample), the General Linear Mixed Model implemented in SAS v.8 (Littell et al. 1996) was applied on log-transformed taxon richness data from 16 publications. A sample consisted of a partial or a full root system of a plant individual; in the 16 publications analysed, there was no multiple sampling per single individual. Habitat type was included in the model as a factor. Four broadly defined habitat types were used: habitats under strong anthropogenic influence (arable fields and polluted habitats), temperate grasslands (grasslands and treeless Phragmites wetlands), temperate forests (deciduous forests and boreal coniferous forests) and tropical forests. The study site was included in the model as a random factor nested within habitat type. In all but a few cases, the investigated host plant species and families did not overlap between studies (Table 1). Therefore, the identity of host plants at class level (monocotyledons or dicotyledons) was included in the model as a random factor. To compensate for differences in sample size, the log-transformed number of root samples was included as a continuous variable. The study site and research team could not simultaneously be included in the model as an independent random factor. The reason for this was the lack of sufficient replication in the number of sites studied by each team (mostly 1–3, with one exception; see Table 1), and hence the effect of the team was indirectly described by the effect of the site. No site had been studied by several teams.

For a comparison of taxon composition between AM fungal communities, cluster analysis was performed on the data matrix of 95 AMF taxa (presence–absence data) in the roots of 36 host plant species (including six species represented only in soil core samples where all roots were pooled) at 25 sites. The Ward clustering method with Euclidean distance was implemented in PC-ORD v.4 (McCune & Mefford 1999). Here a sample (a terminal branch in a cluster diagram) is a list of AM fungal taxa in the roots of a plant species from one study site.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

diversity of am fungal communities

Twenty-six publications were surveyed that reported the occurrence of AM fungal taxa in the roots of plants grown in their native habitats or on native soil in experimental conditions (Table 1). AM fungi had been detected and identified in these studies using small subunit ribosomal RNA gene (SSU rDNA, 17 studies), internal transcribed spacer (ITS, two studies), large subunit ribosomal RNA gene (LSU rDNA, four studies) or both SSU and ITS markers (three studies). A total of 52 host plant species have been investigated, including one liverwort species and seven myco-heterotrophic epiparasitic plant species. Sixteen studies using the SSU rDNA region provided comparable data, reporting on the occurrence of 95 fungal taxa in the roots of 36 plant species (including six species represented only in pooled root samples) across 25 study sites. Forty-nine AM fungal taxa were recorded from at least two study sites, and 65 taxa from more than one host plant species.

Different numbers of AM fungal taxa from a range of ecosystems have been identified (summarized in Table 1). The highest taxon richness in a single study area has been reported in tropical forests in Panama (29 taxa at three sites, Husband et al. 2002a) and in temperate grassland in Japan (24 taxa at two sites, Saito et al. 2004). Only one AM fungal taxon was involved in the strictly specific symbiotic relationships with non-photosynthetic plants and liverworts (Bidartondo et al. 2002; Russell & Bulman 2005).

The Shannon diversity index (H), which takes into account both the number and the relative proportions of taxa in a community, ranged from 0.45 for the AM fungal community in an arable field (Daniell et al. 2001) to 2.58 across two locations of afromontane forest (Wubet et al. 2004; Table 1). These differences indicate the presence of varying levels of dominance in AM fungal communities. In arable fields, Glomus sp. Glo1a comprised 62% of the clones of eight fungal taxa present in those fields (Daniell et al. 2001). In AM fungal communities colonizing Prunus africana in afromontane forest sites, the two most abundant taxa comprised only 18% and 21% of total clones in a community of 20 AM fungal taxa (Wubet et al. 2004).

Within the analysed SSU rDNA dataset, the number of AM fungal taxa per host plant species was significantly affected by habitat type (F3,19 = 5.69, P = 0.006, GLM analysis) and sample size (F1,20 = 13.28, P = 0.002). The average number of AM fungal taxa associated with a host plant species increased from 5.2 in habitats under strong anthropogenic influence, to 5.6 in temperate forests and 8.3 in temperate grasslands, and 18.2 in tropical forests (Fig. 1). Tropical forests exhibited significantly higher AM fungal taxon richness per plant species than habitats under strong anthropogenic influences and temperate forests. In order to assess the robustness of the habitat type effect, the analysis was also performed without the tropical forest data originating from only one forest (Husband et al. 2002a,b). There was no effect of habitat type on fungal taxon richness when a dataset without tropical forest was used. The variation in AM fungal taxon richness could not be explained by the identity of host plants (i.e. mono- or dicotyledons; Z = 0.49, P = 0.31) or by study site (Z = 1.39, P = 0.08).

image

Figure 1. Recorded average number of arbuscular mycorrhizal fungal taxa per host plant species in different types of habitats. The data presented are LS means ± SE. Different letters above bars indicate significant differences between means according to the Sheffe multiple comparison test (P < 0.05). Data on non-photosynthetic plants were not included in this analysis.

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composition of am fungal communities

The multivariate cluster analysis of comparable datasets from 16 publications suggests that the composition of AM fungal communities is related to ecosystem type (Fig. 2). The analysis revealed three clear clusters distinguished at the level of 65% of the information remaining: I, AM fungal communities in the roots of tree seedlings in the tropical rain forest in Panama; II, AM fungal communities from arable fields and polluted soil; and III, AM fungal communities from temperate forests, including a boreal Scots pine forest in Estonia and a deciduous forest in the UK. Grassland samples formed a heterogeneous group, with study-site-specific subclusters, indicating a large variation in fungal community composition among grassland locations.

image

Figure 2. Cluster analysis showing ecosystem-related grouping of arbuscular mycorrhizal (AM) fungal communities. The Ward clustering method with Euclidean distance was used. A branch terminus constitutes an AM fungal community inhabiting the roots of one host plant species in one site. Individual fungal communities are coded by ecosystem, publication and site (as in Table 1) and plant species. Abbreviations: Ac, Agrostis capillaris; Ap, Acer pseudoplatanus; Ar, Ajuga reptans; Ae, Arrhenaterium elatius; Cm, Calpogonium mucunoides; Ce, Cynosurus echinatus; E, Epilobium angustifolium; Foc, Faramea occidentalis; Fov, Festuca ovina; G, Glechoma hederacea; Hp, Hieracium pilosella; Hns, Hyacinthoides non-scripta; Hv, Hordeum vulgare; Lc, Lotus corniculatus; Ls, Luehea seemannii; M, Miscanthus sinensis; O, Ononis repens; pooled, samples of pooled roots from different species; Pa, Phragmites australis; Pl, Plantago lanceolata; Ppa, Pulsatilla patens; Ppr, P. pratensis; Ps, Pisum sativum; R, Rubus fruticosus; Ta, Triticum aestivum; Tpa, Tetragastris panamensis; Tpo, Thymus polytrichus; Tar, Torilis arvensis; Tr, Trifolium repens; Zm, Zea mays; Zj, Zoysia japonica. *Samples from experimental conditions, see Materials and methods. For example, ‘Tropics 4c Tpa’ reads: tropical forest in study 4, site c (Tropical forest site from Husband et al. 2002b) Tetragastris panamensis AM fungal community.

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The same analysis was also performed at the level of study sites (data from host species were pooled for each site), or with the removal of some samples (e.g. samples from sites under strong human impact; samples of experimental plants; some of the samples from each habitat) from the analysis, or with the removal of unique AM fungal taxa. The same three clear groupings and a heterogeneous assemblage of grasslands were evident (data not shown), indicating that the obtained tree topology is robust.

Cluster I is characterized by 11 taxa occurring only in tropical forest: Glomus spp. Glo32–34, 36–38 and 45, Scutellospora sp. Scut4, and Acaulospora spp. Acau8, 10 and 12. Cluster II included four specific taxa: Glomus sp. Glo6 occurred in arable fields only, and Glomus types 2 + 10, 12 and 18 in polluted sites only. Cluster III included five specific taxa: Acaulospora sp. Acau4 and Other1 were found in deciduous forests, and Acaulospora sp. MO-A1, Scutellospora spp. MO-S1 and MO-S2 in boreal coniferous forests. The heterogeneous group of all grasslands contained 33 specific taxa (not listed; Table 2). The most distinguished grassland locations were those in Japan (sites 9L and 9m in Fig. 2), with 14 specific taxa, and two Phragmites wetland locations in Germany, with eight specific taxa.

Table 2.  The occurrence of the 13 most frequently detected AM fungal taxa (SSU rDNA sequence types), and the number of taxa detected only from a particular ecosystem. The values given in the table are the numbers of study sites where the fungal taxon is represented. Synonymous taxon codes are shown in column headings as applied by different authors. D, dominant taxon in any of the surveyed studies
 Taxon code by:‘York group’Glo8Glo1bGlo3aGlo10/ Glo24Glo4Glo17/ Glo53Glo18Glo2Glo9Scut1/ Scut2/ Scut3Glo1aGlo7
  Öpik et al. (2003)G3G11G2  G4 G5G7 G10G6
  Saito et al. (2004)  GloAb3 GloAc1  GloAd3GloAc6   
 Whitfield et al. (2004)type 19, 20, 21type 5, 17 type 7, 11type 4, 15type 6type 3     
  Wirsel (2004)OTU1OTU5 OTU2OTU13, 14, 18OTU8OTU8 OTU7  OTU4
 Related species G. intraradices/fasciculatum G. mosseae Glomus sp. UY1225      G. hoi   C. caldonium  
EcosystemNo. of sites studiedNo. of ecosystem- specific taxa            
Tropical forest 411 4 D 4 4 4  4 D 4412  
Boreal forest 1 1  1 D 1     D 11  1
Deciduous forest 1 3 1  1    11 D 1 1
Grassland (incl. lahar)1033 D 7 1 D 6 D 2 D 3 4 4 D 43443
Wetland 2 8 D 2 2  2 2 2 2 2  2
Polluted sites 3 3  D 3  1 3 1 1     
Arable fields 3 1 3 3  3 3    1 D 3 
Total24 17141212111111108877

distribution patterns of widespread am taxa

Of the 95 AM fungal taxa recorded, 49 had been detected in more than one study site, and 65 in the roots of more than one host plant species (at a site). The occurrence of the 13 most frequently detected taxa in different ecosystems is presented in Table 2. Ten of these taxa were dominant in at least one study site. The most commonly detected, Glomus sp. Glo8 (related to the G. intraradices/fasciculatum group), is known from tropical forests (all sites and host species), in 7 out of 11 grassland sites, from a temperate deciduous forest and from a few arable fields (one host only). It has also been shown to colonize root nodules (Scheublin et al. 2004). Glomus sp. Glo1b (related to G. mosseae) and Glo10 are relatively omnipresent in temperate arable fields and tropical forests, and are sometimes found in grasslands and wetlands, but are absent in temperate broadleaved forests. Glomus spp. Glo2 and Glo3 (the latter is related to undescribed Glomus isolate UY1225) are known in tropical, temperate and boreal forests and temperate grasslands, but not in arable fields, wetland or polluted ecosystems. Glomus sp. Glo1a (related to G. caledonium) and Glo4 seem to be slightly ‘ruderal’ taxa, being common in arable fields, present in grasslands, but absent in tropical, temperate and boreal forests.

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

the number of am fungi varies among ecosystems

A major goal in microbial ecology is to understand whether microbes have a biogeography (Fitter 2005). Until recently, data regarding the distribution of most microbes, including AM fungi, were very scarce. However, an increasing number of molecular surveys present data on the distribution of AM fungi in a number of host plants and ecosystems. The meta-analysis presented herein showed significant between-habitat variation in the number of AM fungal taxa colonizing single plant species. The outstandingly high number of AM fungal taxa in tropical forests contrasted with the both low AM fungal taxon richness and low diversity in arable fields, i.e. the high dominance of a single taxon (Fig. 1; Helgason et al. 1998; Daniell et al. 2001; Husband et al. 2002a,b). The AM fungal communities of non-photosynthetic plants (Bidartondo et al. 2002) and a liverwort Marchantia (Russell & Bulman 2005) also show exceptionally low richness, which indicates highly specific symbiotic relationships. Our analysis also identified an effect of sample size on the number of fungal taxa recorded, suggesting that more exhaustive sampling should be considered in future studies.

The tropical forest data analysed here originate from four locations in a single forest, and might not be representative of a diverse range of tropical forests. In comparison with the root-colonizing taxa, spore communities show similar or slightly lower richness in other wet tropical forests (Lovelock et al. 2003; Mangan et al. 2004), but no richness differences between grasslands and dry tropical forests (Johnson & Wedin 1997), or between a subtropical forest and deforested site (Zhang et al. 2004). Nevertheless, management intensity was shown to reduce species richness in temperate arable fields and grasslands (Oehl et al. 2003).

the number of am fungal sequence types is high

The number of root-colonizing AM fungal SSU rDNA sequence types (taxa) overviewed here – 95 taxa detected from 25 locations, based on 16 studies – on the background of c. 150 described Glomeromycota species provides further support to the view that there is still a large undiscovered diversity of Glomeromycota (Helgason et al. 2002; Fitter 2005). This number of (sequence-based) AM fungal taxa detected by independent investigators is steadily increasing. Approximately one-third of such taxa can be related to taxonomically described and named fungi, whereas others are known only as sequence types, either previously detected from other locations/by other authors or new types.

In addition to natural variation, the importance of methodological artefacts in generating such diversity should not be forgotten. For instance, chimeric sequences or those containing other PCR/cloning/sequencing errors may potentially contribute to the growing body of ‘unknown’ and rare taxa. In order to minimize such bias, the dataset analysed here was carefully checked for the identification of synonymous sequence types, and authors’ original sequence types were combined instead of being further divided. Furthermore, several authors report checking for chimeras and the removal of obvious artefacts from their data sets before analysis (e.g. see Vandenkoornhuyse et al. 2002b; Öpik et al. 2003). Therefore, the proportion of artefact sequence groups in the analysed dataset is probably negligible.

Another methodological issue affecting the number of taxa detected is the group delimitation of environmental sequences based on phylogenetic analysis. The range of reference sequences available in sequence databases may affect the outcome of phylogenetic sequence analysis. Furthermore, defining the groups of sequences as ‘types’ is dependent on pre-existing knowledge of the intra- and interspecific genetic variation of the study organisms and also on the investigator's decision concerning where to draw the line between the groups. A similarity level of 97% has been used as a lower boundary in defining groups (Helgason et al. 1999). There is evidence of high intraspecific and intra-individual genetic variation in some groups (see Sanders 2002; Pawlowska & Taylor 2004; Rodriguez et al. 2004; Rosendahl & Stukenbrock 2004). This obviously sets limits on the reliability of sequence types as used in the above studies and on the possibilities of linking the sequence types detected from field samples with morphologically described species possessing known functional properties (Sanders 2004). The recently highlighted intraspecific functional diversity (Hart & Reader 2002; Munkvold et al. 2004) calls for further revision of Glomeromycota taxonomy based on functional genes (van der Heijden et al. 2004).

amf community patterns in ecosystems

Studies conducted at the local scale have suggested that the taxonomic composition of and dominant AM fungal taxa colonizing plant roots may differ between habitat types, host species and locations in the root system (nodules vs. roots per se) (Helgason et al. 1998, 1999, 2002; Daniell et al. 2001; Husband et al. 2002a,b; Öpik et al. 2003; Heinemeyer et al. 2004; Scheublin et al. 2004; Wirsel 2004; Wubet et al. 2004). Conventional spore-based investigations provide evidence that the distribution of AM fungal spores in soil can be affected by biotic and abiotic factors, such as host plant species, ecosystem type, soil pH, soil moisture, total soil C and N, temperature, season and disturbance regime (Schenck & Kinloch 1980; McGraw & Hendrix 1984; Koske 1987; Gibson & Hetrick 1988; Johnson et al. 1991, 1992; Boddington & Dodd 2000; Egerton-Warburton & Allen 2000; Carvalho et al. 2003). The meta-analysis presented offers further support to the importance of habitat type as a factor influencing AM fungal community composition on a larger spatial scale. We are not aware of any spore-based meta-analyses that would make it possible to validate this finding.

A distinction of AM fungal communities from certain broad habitat types – tropical forests, temperate forests and habitats under strong anthropogenic influence – was indicated by the cluster analysis (Fig. 2). The clustering of temperate grasslands, however, resulted in a rather heterogeneous group of AM fungal communities, which can be explained by the largest number of studies conducted in distant geographical locations (Japan, Estonia, Netherlands, UK, USA) and in quite different ecological conditions. The results from the most intensively studied country, the UK, also make the interhabitat difference of AM fungal communities visible–polluted sites, arable fields, deciduous forest and grasslands differ significantly from one another. Read (1991) has provided a broad overview of changes of a predominating mycorrhizal type in different biomes. Our data show that within the AM-dominated biomes the composition of AM fungal communities may differ between regions and habitat types. In addition, there were evident differences between ecosystems under different disturbance regimes.

The host effect on AM fungal communities was not evident in our analysis because too few studies contained data on the fungal communities of the same plant species at different sites. Öpik et al. (2003) studied AM fungal communities in the roots of two plant species grown on soils from two different habitat types, a boreal forest and a temperate grassland. The AM fungal community composition in the roots of Pulsatilla patens and P. pratensis fell in respective clusters of grassland and forest fungal communities (communities ‘Boreal 1a’ and ‘Grassland 1i/1j’ in Fig. 2). The AM fungal communities of Phragmites australis from two wetland locations (Wirsel 2004) appear as a distinct cluster among grassland clusters; the fungal communities of Trifolium repens from the UK (Vandenkoornhuyse et al. 2002b) and the Netherlands (Scheublin et al. 2004) appear in the clusters of the respective grassland sites (grasslands 10n and 6g, Fig. 2). However, investigations of the same plant species in different locations deserve further attention in order to test the habitat/location vs. host effect on fungal community composition.

Despite the high diversity of host plant species investigated in the surveyed publications, the between-habitat variation in AM fungal communities remains obvious, indicating that ecosystem type is possibly a more important determinant of AM fungal community composition than host species identity at this level of resolution.

distribution of am fungal taxa

The global survey of AM fungal taxa presented here suggests that within Glomeromycota, different distribution patterns occur: some taxa show a global range, others are limited to a few ecosystems only, and a considerable number of taxa are rarely reported.

About half of the surveyed AM fungal taxa were detected from one site only, and about one-third were recorded from only one host plant species. At the same time, globally frequent species were also locally abundant in at least some study sites (Table 2). The rare and site-specific taxa were not dominant in the studied ecosystems, except Glomus type GloAb2, specific to two grassland locations in Japan (Saito et al. 2004). However, even if not frequent, most of the site- or host-specific taxa have been detected more than once, suggesting that these are real types and not methodological artefacts.

The question of whether there are rare soil microbes and whether there is a risk of the extinction of such organisms was recently presented by Fitter (2005). Regarding the large proportion of rarely reported AM fungal sequence types, the amount of data does not allow us to say whether these types are rare or whether their real frequency has not been properly revealed. The composition and diversity of AM fungal communities may related to the host species, the life stage of the host plant, the season or the specific site conditions (Helgason et al. 2002; Husband et al. 2002b; Vandenkoornhuyse et al. 2002b; Öpik et al. 2003; Scheublin et al. 2004). Therefore, many rarely reported taxa may actually be confined to specific conditions or grow in a spatially fragmented manner. Better defined sampling strategies, possibly tailored to each location/system and research problem, would allow future descriptive studies to assess better the real frequency of AM fungi.

The established global distribution of some AM fungi raises the question of whether these taxa are functionally homogeneous (van der Heijden et al. 2004). The functional characteristics of the AM fungi detected in field samples are largely unknown because most of these taxa have not been isolated in culture and may not be presently cultivatable (see Helgason et al. 2002; Fitter 2005). Even information regarding the cultured species is scarce. Functional diversification among isolates of the same species from distant localities has recently been suggested on the basis of the differential effect on plant growth (Hart & Reader 2002; Munkvold et al. 2004) or different hyphal length (Koch et al. 2004). Contradictory evidence of the spore dormancy of G. mosseae isolates reporting either no dormancy or a need for storage at low positive or negative temperatures to induce germination (Hepper & Smith 1976; Safir et al. 1990; Douds & Schenck 1991) could also be explained through adaptation to local climatic conditions, and thus show functional variation within species. The cultivability of the three most common species according to the present overview, Glomus intraradices, G. mosseae and G. sp. UY1225, offers optimism that enlightening results will soon be obtained.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

The presented meta-analysis of AM fungal communities across a selection of worldwide locations and ecosystems suggests that soil micro-organisms such as AM fungi may exhibit different distribution patterns, including taxa that are common, specific to a region/ecosystem and possibly rare. Data from a wider range of ecosystems with more replication in locations and plant host species is expected to increase the number of AM fungal taxa even further. We expect the present study of broad biodiversity patterns of AM fungal distribution to assist in establishing the link between AM fungal sequence type assemblages and ecosystem function. As recently proposed, it may be genetic diversity, either within or among AM fungal species, rather than the species richness of AM fungi that has implications for plant diversity and thus for ecosystem function (Sanders 2004).

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

This work was supported by Estonian Science Foundation grant no. 6533 and EU FP6 integrated project ALARM (contract 506675).

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References