Skip to main content
Log in

Arbuscular mycorrhizal community structure on co-existing tropical legume trees in French Guiana

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

We aimed to characterise the arbuscular mycorrhizal fungal (AMF) community structure and potential edaphic determinants in the dominating, but poorly described, root-colonizing Paris-type AMF community on co-occurring Amazonian leguminous trees.

Methods

Three highly productive leguminous trees (Dicorynia guianensis, Eperua falcata and Tachigali melinonii were targeted) in species-rich forests on contrasting soil types at the Nouragues Research Station in central French Guiana. Abundant AMF SSU rRNA amplicons (NS31-AM1 & AML1-AML2 primers) from roots identified via trnL profiling were subjected to denaturing gradient gel electrophoresis (DGGE), clone library sequencing and phylogenetic analysis.

Results

Classical approaches targeting abundant SSU amplicons highlighted a diverse root-colonizing symbiotic AMF community dominated by members of the Glomeraceae. DGGE profiling indicated that, of the edaphic factors investigated, soil nitrogen was most important in influencing the AMF community and this was more important than any host tree species effect.

Conclusions

Dominating Paris-type mycorrhizal leguminous trees in Amazonian soils host diverse and novel taxa within the Glomeraceae that appear under edaphic selection in the investigated tropical forests. Linking symbiotic diversity of identified AMF taxa to ecological processes is the next challenge ahead.

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

Similar content being viewed by others

References

  • Aime MC, Brearley FQ (2012) Tropical fungal diversity: closing the gap between species estimates and species discovery. Biodivers Conserv 21:2177–2180. doi:10.1007/s10531-012-0338-7

  • Aldrich-Wolfe L (2007) Distinct mycorrhizal communities on new and established hosts in a transitional tropical plant community. Ecology 88:559–566. doi:10.1890/05-1177

    Article  PubMed  Google Scholar 

  • Alexander IJ (1989) Mycorrhizas in tropical forests. In: Proctor J (ed) Mineral nutrients in tropical forest and savanna ecosystems. Blackwell Scientific Publications, Oxford, UK, pp. 169–188

    Google Scholar 

  • Béreau M, Garbaye J (1994) First observations on the root morphology and symbioses of 21 major tree species in the primary tropical rain forest of French Guyana. Ann Sci For 51:407–416. doi:10.1051/forest:19940406

    Article  Google Scholar 

  • Béreau M, Louisanna E, Garbaye J (2004) Mycorrhizal symbiosis in the tropical rainforest of French Guiana and its potential contribution to tree regeneration and growth. In: Ecology and management of a neotropical rainforest. In: S Gourlet-Fleu (eds), J-M Guehl, O laroussinie). Elsevier, Paris, France, pp. 114–119

    Google Scholar 

  • Bongers F, Charles-Dominique P, Forget PM, Théry M (2001) Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer Academic Publishers, Dordrect, The Netherlands

    Book  Google Scholar 

  • Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659. doi:10.1111/gcb.12618

    Article  PubMed  Google Scholar 

  • CBOL Plant Working Group (2009) A DNA barcode for land plants. Proc Natl Acad Sci U S A 106:12794–12797. doi:10.1073/pnas.0905845106

    Article  PubMed Central  Google Scholar 

  • Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples version 9. http://purl.oclc.org/estimates .

  • de Grandcourt A, Epron D, Montpied P, Louisanna E, Béreau M, Garbaye J, Guehl J-M (2004) Contrasting responses to mycorrhizal inoculation and phosphorus availability in seedlings of two tropical rainforest tree species. New Phytol 161:865–875. doi:10.1046/j.1469-8137.2004.00978.x

    Article  Google Scholar 

  • de Oliveira FR, Buscardo E, Nagy L, dos Santos Maciel AB, Carrenho R, Luizão RCC (2014) Arbuscular mycorrhizal fungal communities along a pedo-hydrological gradient in a central Amazonian terra firme forest. Mycorrhiza 24:21–32. doi:10.1007/s00572-013-0507-x

    Article  Google Scholar 

  • Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167. doi:10.1146/annurev.energy.28.050302.105532

    Article  Google Scholar 

  • Dumbrell AJ, Nelson M, Dytham C, Helgason T, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME j 4:337–345. doi:10.1038/ismej.2009.122

    Article  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  • Elliott DR, Wilson M, Buckley CMF, Spratt DA (2005) Cultivable oral microbiota of domestic dogs. J Clin Microbiol 43:5470–5476. doi:10.1128/JCM.43.11.5470-5476.2005

    Article  PubMed  PubMed Central  Google Scholar 

  • Fauset S et al. (2015) Hyperdominance in Amazonian forest carbon cycling. Nat Commun 6:6857. doi:10.1038/ncomms7857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fitzsimons MS, Miller RM, Jastrow JD (2008) Scale-dependent niche axes of arbuscular mycorrhizal fungi. Oecologia 158:117–127. doi:10.1007/s00442-008-1117-8

    Article  PubMed  Google Scholar 

  • Gallaud I (1904) Études sur les mycorrhizes endotrophes. Le Bigot Frères, Lille, France

    Google Scholar 

  • Ghazoul J, Sheil D (2010) Tropical rain forest ecology, diversity, and conservation. Oxford University Press, UK

    Google Scholar 

  • Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJA, Laurance WF, Lovejoy TE, Sodhi NS (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478:378–381. doi:10.1038/nature10425

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez MA, Baraloto C, Engel J, Mori SA, Pétronelli P, Riéra B, Roger A, Thébaud C, Chave J (2009) Identification of Amazonian trees with DNA barcodes. PLoS One 4:e7483. doi:10.1371/journal.pone.0007483

    Article  PubMed  PubMed Central  Google Scholar 

  • Haug I, Setaro S, Suárez JP (2013) Reforestation sites show similar and nested AMF communities to an adjacent pristine forest in a tropical mountain area of south Ecuador. PLoS One 8:e63524. doi:10.1371/journal.pone.0063524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haug I, Wubet T, Weiß M, Aguirre N, Weber M, Günter S, Kottke I (2010) Species-rich but distinct arbuscular mycorrhizal communities in reforestation plots on degraded pastures and in neighboring pristine tropical mountain rain forest. Trop Ecol 51:125–148

    CAS  Google Scholar 

  • Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME j 7:498–508. doi:10.1038/ismej.2012.127

  • Heinonsalo J, Jørgensen KS, Sen R (2001) Microcosm-based analyses of Scots pine seedling growth, ectomycorrhizal fungal community structure and bacterial carbon utilization profiles in boreal forest humus and underlying illuvial mineral horizons. FEMS Microbiol Ecol 36:73–84. doi:10.1111/j.1574-6941.2001.tb00827.x

    Article  CAS  PubMed  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431. doi:10.1038/28764

    Article  CAS  PubMed  Google Scholar 

  • Helgason T, Merryweather JW, Young JPW, Fitter AH (2007) Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. J Ecol 95:623–630. doi:10.1111/j.1365-2745.2007.01239.x

    Article  CAS  Google Scholar 

  • Hepper CM, Azcon-Aguilar C, Rosendahl S, Sen R (1988) Competition between three species of Glomus used as spatially separated introduced and indigenous mycorrhizal inocula for leek (Allium porrum L.). New Phytol 110:207–215. doi:10.1111/j.1469-8137.1988.tb00254.x

    Article  Google Scholar 

  • Hodge A (2014) Interactions between arbuscular mycorrhizal fungi and organic material substrates. Adv Appl Microbiol 89:47–99. doi:10.1016/B978-0-12-800259-9.00002-0

    Article  PubMed  Google Scholar 

  • Huang X (1992) A contig assembly program based on sensitive detection of fragment overlaps. Genomics 14:18–25. doi:10.1016/S0888-7543(05)80277-0

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682. doi:10.1093/bioinformatics/btq003

    Article  CAS  PubMed  PubMed Central  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. doi:10.1046/j.1365-294X.2002.01647.x

    Article  CAS  PubMed  Google Scholar 

  • Ji B, Bentivenga SP, Caspar BB (2012) Comparisons of AM fungal spore communities with the same hosts but different soil chemistries over local and geographical scales. Oecologia 168:187–197. doi:10.1007/s00442-011-2067-0

    Article  PubMed  Google Scholar 

  • Jones FA, Erickson DL, Bernal MA, Bermingham E, Kress WJ, Herre EA, Muller-Landau HC, Turner BL (2011) The roots of diversity: below ground species richness and rooting distributions in a tropical forest revealed by DNA barcodes and inverse modeling. PLoS One 6:e24506. doi:10.1371/journal.pone.0024506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiers ET, Lovelock CE, Krueger EL, Herre EA (2000) Differential effects of tropical arbuscular mycorrhizal fungal inocula on root colonization and tree seedling growth: implications for tropical forest diversity. Ecol Lett 3:106–113. doi:10.1046/j.1461-0248.2000.00126.x

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. doi:10.1016/j.soilbio.2011.07.012

    Article  CAS  Google Scholar 

  • Koch AM, Croll D, Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecol Lett 9:103–110. doi:10.1111/j.1461-0248.2005.00853.x

    Article  PubMed  Google Scholar 

  • Kohout P, Sudová R, Janoušková M, Čtvrtlíková M, Hejda M, Pánková H, Slavíková R, Štajerová K, Vosátka M, Sýkorová Z (2014) Comparison of commonly used primer sets for evaluation of arbuscular mycorrhizal fungal communities: is there a universal solution? Soil Biol Biochem 68:482–493. doi:10.1016/j.soilbio.2013.08.027

    Article  CAS  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349. doi:10.1111/j.1574-6941.2008.00531.x

    Article  CAS  PubMed  Google Scholar 

  • Lovelock CE, Andersen K, Morton JB (2003) Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia 135:268–279. doi:10.1007/s00442-002-1166-3

    Article  PubMed  Google Scholar 

  • Martin J, Béreau M, Louisanna E, Ocampo JA (2001) Arbuscular mycorrhizas in Dicorynia guianensis and Eperua falcata trees from primary tropical rain forest of French Guiana. Symbiosis 31:283–291

    Google Scholar 

  • Michalet S, Rohr J, Warshan D, Bardon C, Roggy J-C, Domenach A-M, Czarnes S, Pommier T, Combourieu B, Guillaumand N, Bellvert F, Comte G, Poly F (2013) Phytochemical analysis or mature tree root exudates in situ and their role in shaping soil microbial communities in relation to tree N-acquisition strategy. Plant Physiol Biochem 72:169–177. doi:10.1016/j.plaphy.2013.05.003

    Article  CAS  PubMed  Google Scholar 

  • Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027. doi:10.1016/j.soilbio.2007.11.014

    Article  CAS  Google Scholar 

  • Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364. doi:10.1111/j.1469-8137.2004.01169.x

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. (2015) Vegan: community ecology package. R Package version 2.2–1. http://cran.r-project.org/package=vegan

    Google Scholar 

  • Öpik M, Moora M, Liira J, Kõljalg U, Zobel M, Sen R (2003) Divergent arbuscular mycorrhizal fungal communities colonize roots of Pulsatilla spp. in boreal scots pine forest and grassland soils. New Phytol 160:581–593. doi:10.1046/j.1469-8137x.2003.00917.x

    Article  Google Scholar 

  • 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. doi:10.1111/j.1469-8137.2010.03334.x

    Article  PubMed  Google Scholar 

  • 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 23:411–430. doi:10.1007/s00572-013-0482-2

    Article  PubMed  Google Scholar 

  • Paradis E, Claude G, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. doi:10.1093/bioinformatics/btg412

    Article  CAS  PubMed  Google Scholar 

  • Pizano C, Mangan SA, Herre EA, Eom AH, Dalling JW (2011) Above- and belowground interactions drive habitat segregation between two cryptic species of tropical trees. Ecology 92:47–56. doi:10.1890/09-1715.1.

    Article  PubMed  Google Scholar 

  • Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139. doi:10.1093/treephys/tpq063.

    Article  CAS  PubMed  Google Scholar 

  • Poszwa A, Ferry B, Pollie B, Grimaldi C, Charles-Dominique P, Loubet M, Dambrine E (2009) Variations of plant and soil 87Sr/86Sr along the slope of a tropical inselberg. Ann For Sci 66:512. doi:10.1051/forest/2009036

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

    Google Scholar 

  • Ridgway KP, Duck JM, Young JPW (2003) Identification of roots from grass swards using PCR-RFLP and FFLP of the plastid trnL (UAA) intron. BMC Ecol 3:8. doi:10.1186/1472-6785-3-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Roger A, Colard A, Angelard C, Sanders IR (2013) Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME j 7:2137–2146. doi:10.1038/ismej.2013.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schimann H, Ponton S, Hättenschwiler S, Ferry B, Lensi R, Domenach A-M, Roggy J-C (2008) Differing nitrogen use strategies of two tropical rainforest late successional tree species in French Guiana: evidence from 15N natural abundance and microbial activities. Soil Biol Biochem 40:487–494. doi:10.1016/j.soilbio.2007.09.011

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. doi:10.1038/nmeth.2089

    Article  CAS  PubMed  Google Scholar 

  • Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145. doi:10.1038/nbt1486

    Article  CAS  PubMed  Google Scholar 

  • Sheublin TR, Ridgway KR, Young JPW, van der Heijden MGA (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246. doi:10.1128/AEM.70.10.6240-6246.2004.

    Article  Google Scholar 

  • Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular–arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slik JWF et al. (2015) An estimate of the number of tropical tree species. Proc Natl Acad Sci U S A 112:7272–7477. doi:10.1073/pnas.1423147112

    Article  Google Scholar 

  • Smith FA, Smith SE (1997) Structural diversity in (vesicular-)arbuscular mycorrhizal symbioses. New Phytol 137:373–388

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York, USA

    Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, UK

    Google Scholar 

  • Stürmer SL, Siqueira JO (2011) Species richness and spore abundance of arbuscular mycorrhizal fungi across distinct land uses in western Brazilian amazon. Mycorrhiza 21:255–267. doi:10.1007/s00572-010-0330-6

    Article  PubMed  Google Scholar 

  • Sýkorová Z, Wiemken A, Redecker D (2007) Cooccurring Gentiana Verna and Gentiana acaulis and their neighboring plants in two Swiss upper montane meadows harbor distinct arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 73:5426–5434. doi:10.1128/AEM.00987-07

    Article  PubMed  PubMed Central  Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109. doi:10.1007/BF00037152

    Article  CAS  PubMed  Google Scholar 

  • ter Steege H, Pitman NCA, Phillips OL, Chave J, Sabatier D, Duque A, Molino J-F, Prévost M-F, Spichiger R, Castellanos H, von Hildebrand P, Vásquez R (2006) Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443:444–447. doi:10.1038/nature05134

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091. doi:10.1890/0012-9658(1998)079[2082:DAMFSA]2.0.CO;2

    Article  Google Scholar 

  • van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology: the past, the present, and the future. New Phytol 205:1406–1423. doi:10.1111/nph.13288

    Article  PubMed  Google Scholar 

  • Werner GDA, Kiers ET (2015) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205:1515–1524. doi:10.1111/nph.13092

    Article  CAS  PubMed  Google Scholar 

  • Zeng W, Zou B, Lei P, Zeng Y, Liu Y, Liu C, Xiang W (2015) A molecular method to identify species of fine roots and to predict the proportion of a species in mixed samples in subtropical forests. Front Plant Sci 6:313. doi:10.3389/fpls.2015.00313

Download references

Acknowledgments

We thank Centre National de la Recherche Scientifique for managing the Nouragues Research Station and funding this study through Project Amazonie and Manchester Metropolitan University for providing a research assistantship to DRE. We are very grateful to Jérôme Chave for his support of this project and Philippe Gaucher and Patrick Châtelet who were of great help during fieldtrip preparation and sampling. Maarja Öpik provided advice on AMF phylogeny and Stavros Veresoglou, John Davison and anonymous reviewers are thanked for their comments on the manuscript. This project was also partly funded from “Investissement d’Avenir” grants managed by Agence Nationale de la Recherche (CEBA: ANR-10-LABX-25-01 and ANAEE-France: ANR-11-INBS-0001).

Author contributions

Designed the study and obtained funding: FQB & RS; performed the study: FQB, DRE & AI; analysed the data: DRE & FQB; wrote the manuscript: FQB, RS & DRE.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francis Q. Brearley.

Additional information

Responsible Editor: Antony Van der Ent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brearley, F.Q., Elliott, D.R., Iribar, A. et al. Arbuscular mycorrhizal community structure on co-existing tropical legume trees in French Guiana. Plant Soil 403, 253–265 (2016). https://doi.org/10.1007/s11104-016-2818-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-2818-0

Keywords

Navigation