Advertisement

Fungal, Bacterial, and Archaeal Diversity in Soils Beneath Native and Introduced Plants in Fiji, South Pacific

  • Gian Maria Niccolò Benucci
  • Victor Bonito
  • Gregory Bonito
Soil Microbiology

Abstract

The Fiji Islands is an archipelago of more than 330 islands located in the tropics of the South Pacific Ocean. Microbial diversity and biogeography in this region is still not understood. Here, we present the first molecular characterization of fungal, bacterial, and archaeal communities in soils from different habitats within the largest Fijian island, Viti Levu. Soil samples were collected from under native vegetation in maritime-, forest-, stream-, grassland-, and casuarina-dominated habitats, as well as from under the introduced agricultural crops sugarcane, cassava, pine, and mahogany. Soil microbial diversity was analyzed through MiSeq amplicon sequencing of 16S (for prokaryotes), ITS, LSU ribosomal DNA (for fungi). Prokaryotic communities were dominated by Proteobacteria (~ 25%), Acidobacteria (~ 19%), and Actinobacteria (~ 17%), and there were no indicator species associated with particular habitats. ITS and LSU were congruent in β-diversity patterns of fungi, and fungal communities were dominated by Ascomycota (~ 57–64%), followed by Basidiomycota (~ 20–23%) and Mucoromycota (~ 10%) according to ITS, or Chytridiomycota (~ 9%) according to LSU. Indicator species analysis of fungi found statistical associations of Cenococcum, Wilcoxina, and Rhizopogon to Pinus caribaea. We hypothesize these obligate biotrophic fungi were co-introduced with their host plant. Entoloma was statistically associated with grassland soils, and Fusarium and Lecythophora with soils under cassava. Observed richness varied from 65 (casuarina) to 404 OTUs (cassava) for fungi according to ITS region, and from 1268 (pine) to 2931 OTUs (cassava) for bacteria and archaea. A major finding of this research is that nearly 25% of the fungal OTUs are poorly classified, indicative of novel biodiversity in this region. This preliminary survey provides important baseline data on fungal, bacterial, and archaeal diversity and biogeography in the Fiji Islands.

Keywords

Fiji Islands Soil microbiome Mycorrhizal fungi ITS MiSeq UPARSE LSU rDNA 

Notes

Acknowledgements

We are grateful to the Fijian land-owning clans of the Vanua Davutukia, Korolevu-i-wai who allowed us access to their land to collect samples. We thank Jon Dahl from the Soil and Plant Nutrient Laboratory at Michigan State University for assistance.

Author Contribution

G. B. and V. B. designed the research, sampled the soils in Fiji, and wrote the manuscript. G. M. N. B. extracted DNA, prepared the Illumina library, analyzed the data, and wrote the manuscript. All authors approved the final version for submission.

Funding Information

GMNB and GB acknowledge support from Michigan State University AgBioResearch NIFA project MICL02416 and National Science Foundation (NSF) DEB1737898.

Supplementary material

248_2018_1266_MOESM1_ESM.pdf (68 kb)
Figure S1 Bar plots of relative abundance, based on ITS, LSU and 16S rDNA genes, at ordinal-level. For 16S only the first 50 taxa are shown. Habitats dominated by introduced plant hosts are denoted in bold. (PDF 68 kb)
248_2018_1266_MOESM2_ESM.pdf (234 kb)
Figure S2 Shepard diagrams for ITS, LSU and 16S NMDS graphs reported in Fig. 3. The plot shows of ordination distances against original dissimilarities. Non-metric fit is based on stress value of the NMDS ordination and calculated as R2 = 1-S*S. Linear fit is the squared correlation between fitted values and ordination distances. (PDF 234 kb)
248_2018_1266_MOESM3_ESM.pdf (10 kb)
Figure S3 ITS and LSU NMDS ordinations (Bray-Curtis distance) comparison using Procrustes rotation. Superimposition and residual plots are showed. (PDF 9.97 kb)
248_2018_1266_MOESM4_ESM.pdf (29 kb)
Figure S4 Boxplot of distance to centroids of every sampling location (i.e., site) for ITS, LSU and 16S rDNA. A p value from ANOVA of the distances to group centroids is also reported (perm. = 9999), to test if one or more sample group at each site is more variable than the others. Sites dominated by introduced plant hosts are denoted in bold. (PDF 29.3 kb)
248_2018_1266_MOESM5_ESM.xlsx (15 kb)
Table S1 List of the first 10 top abundant fungal OTUs detected in each of the 18 sites sampled. Taxonomy assignment using RDP classifiers against the UNITE database, taxonomy assignment using BLAST against GenBank database (https://www.ncbi.nlm.nih.gov/genbank/), max score, total score, query coverage, % sequence identity, e-value and sequence reference ID of the best match are reported. (XLSX 14.5 kb)
248_2018_1266_MOESM6_ESM.xlsx (321 kb)
Dataset 1 ITS rDNA otu_table (XLSX 321 kb)
248_2018_1266_MOESM7_ESM.xlsx (248 kb)
Dataset 2 LSU rDNA otu_table (XLSX 247 kb)
248_2018_1266_MOESM8_ESM.xlsx (1.5 mb)
Dataset 3 16S rDNA otu_table (XLSX 1499 kb)
248_2018_1266_MOESM9_ESM.xlsx (360 kb)
Database 1 Herbarium fungal specimen collections of Fiji. (XLSX 359 kb)

References

  1. 1.
    Neall VE, Trewick SA (2008) The age and origin of the Pacific islands: a geological overview. Philos Trans R Soc Lond Ser B Biol Sci 363:3293–3308.  https://doi.org/10.1098/rstb.2008.0119 CrossRefGoogle Scholar
  2. 2.
    Neall VE, Trewick SA (2008) The age and origin of the Pacific islands: a geological overview. Philos Trans R Soc Lond Ser B Biol Sci 363:3293–3308.  https://doi.org/10.1098/rstb.2008.0119 CrossRefGoogle Scholar
  3. 3.
    Ash J (1992) Vegetation ecology of Fiji: past, present, and future perspectives. Retrieved from http://scholarspace.manoa.hawaii.edu/bitstream/10125/718/1/v46n2-111-127.pdf
  4. 4.
    Cown DJ (1981) Wood density of Pinus caribaea var. hondurensis grown in Fiji. N Z J For Sci 11(3):244–253Google Scholar
  5. 5.
    Keppel G, Rounds IA, Thomas NT (2006) The flora, vegetation, and conservation value of mesic forest at Dogotuki, Vanua Levu, Fiji Islands. N Z J Bot 44:273–292.  https://doi.org/10.1080/0028825X.2006.9513024 CrossRefGoogle Scholar
  6. 6.
    Dingley JM (1981) Records of fungi, bacteria, algae, and angiosperms pathogenic on plants in Cook Islands, Fiji, Kiribati, Niue, Tonga, Tuvalu, and Western Samoa. Survey of agricultural pests and diseases. Tech Rep NAVTRADEVCEN 2:1–470Google Scholar
  7. 7.
    Marín DH, Romero RA, Guzmán M, Sutton TB (2003) Black Sigatoka: an increasing threat to banana cultivation. Plant Dis 87:208–222.  https://doi.org/10.1094/PDIS.2003.87.3.208 CrossRefGoogle Scholar
  8. 8.
    Kohlmeyer J, Volkmann-Kohlmeyer B (1987) Marine fungi from Aldabra, the Galapagos, and other tropical islands. Can J Bot 65:571–582.  https://doi.org/10.1139/b87-073 CrossRefGoogle Scholar
  9. 9.
    Kohlmeyer J (1984) Tropical marine fungi. Mar Ecol 5:329–378CrossRefGoogle Scholar
  10. 10.
    Hall N (2007) Advanced sequencing technologies and their wider impact in microbiology. J Exp Biol 210:1518–1525.  https://doi.org/10.1242/jeb.001370 CrossRefPubMedGoogle Scholar
  11. 11.
    Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688.  https://doi.org/10.1126/science.1256688 CrossRefPubMedGoogle Scholar
  12. 12.
    Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liao HL, Smith ME, Peay KG (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci U S A 111:6341–6346.  https://doi.org/10.1073/pnas.1402584111 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Nemergut DR, Costello EK, Hamady M et al (2011) Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13:135–144.  https://doi.org/10.1111/J.1462-2920.2010.02315.X CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631.  https://doi.org/10.1073/pnas.0507535103 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Hejda M, Pyšek P, Pergl J, Sádlo J, Chytrý M, Jarošík V (2009) Invasion success of alien plants: do habitat affinities in the native distribution range matter? Glob Ecol Biogeogr 18:372–382.  https://doi.org/10.1111/j.1466-8238.2009.00445.x CrossRefGoogle Scholar
  16. 16.
    Robertson SJ, Rutherford PM, Massicotte HB (2011) Plant and soil properties determine microbial community structure of shared Pinus-Vaccinium rhizospheres in petroleum hydrocarbon contaminated forest soils. Plant Soil 346:121–132.  https://doi.org/10.1007/s11104-011-0802-2 CrossRefGoogle Scholar
  17. 17.
    Bonito G, Reynolds H, Robeson 2nd MS et al (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol Ecol 23:3356–3370.  https://doi.org/10.1111/mec.12821 CrossRefPubMedGoogle Scholar
  18. 18.
    Coats VC, Rumpho ME (2014) The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants. Front Microbiol 5:368.  https://doi.org/10.3389/fmicb.2014.00368 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nat Methods 10:999–1002.  https://doi.org/10.1038/nmeth.2634 CrossRefPubMedGoogle Scholar
  20. 20.
    Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620.  https://doi.org/10.1093/bioinformatics/btt593 CrossRefGoogle Scholar
  21. 21.
    Caporaso JG, Gregory Caporaso J, Kuczynski J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17:10.  https://doi.org/10.14806/ej.17.1.200 CrossRefGoogle Scholar
  23. 23.
    Edgar RC, Flyvbjerg H (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482.  https://doi.org/10.1093/bioinformatics/btv401 CrossRefPubMedGoogle Scholar
  24. 24.
    Edgar, R. (2016). UCHIME2: improved chimera prediction for amplicon sequencing.  https://doi.org/10.1101/074252
  25. 25.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefPubMedGoogle Scholar
  26. 26.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rDNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267.  https://doi.org/10.1128/AEM.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AF, Tedersoo L, Vrålstad T, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068.  https://doi.org/10.1111/j.1469-8137.2005.01376.x CrossRefPubMedGoogle Scholar
  28. 28.
    DeSantis TZ, Hugenholtz P, Larsen N et al (2006) Greengenes, a chimera-checked 16S rDNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072.  https://doi.org/10.1128/AEM.03006-05 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248.  https://doi.org/10.1016/j.funeco.2015.06.006 CrossRefGoogle Scholar
  30. 30.
    McDonald D, Clemente JC, Kuczynski J, Rideout JR, Stombaugh J, Wendel D, Wilke A, Huse S, Hufnagle J, Meyer F, Knight R, Caporaso JG (2012) The Biological Observation Matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome. Gigascience 1:7.  https://doi.org/10.1186/2047-217X-1-7 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Retrieved from https://www.R-project.org/ Google Scholar
  32. 32.
    Oliver AK, Callaham MA, Jumpponen A (2015) Soil fungal communities respond compositionally to recurring frequent prescribed burning in a managed southeastern US forest ecosystem. For Ecol Manag 345:1–9.  https://doi.org/10.1016/j.foreco.2015.02.020 CrossRefGoogle Scholar
  33. 33.
    Lindahl BD, Henrik Nilsson R, Tedersoo L et al (2013) Fungal community analysis by high-throughput sequencing of amplified markers - a user’s guide. New Phytol 199:288–299.  https://doi.org/10.1111/nph.12243 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Simpson EH (1949) Measurement of diversity. Nature 163:688–688.  https://doi.org/10.1038/163688a0 CrossRefGoogle Scholar
  35. 35.
    Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432.  https://doi.org/10.2307/1934352 CrossRefGoogle Scholar
  36. 36.
    McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217.  https://doi.org/10.1371/journal.pone.0061217 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Langfeldt D, Neulinger SC, Heuer W, Staufenbiel I, Künzel S, Baines JF, Eberhard J, Schmitz RA (2014) Composition of microbial oral biofilms during maturation in young healthy adults. PLoS One 9:e87449.  https://doi.org/10.1371/journal.pone.0087449 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219.  https://doi.org/10.3354/meps092205 CrossRefGoogle Scholar
  39. 39.
    Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. https://doi.org/10.1890/0012-9658(2003)084[0511:caopca]2.0.co;2CrossRefGoogle Scholar
  40. 40.
    Peres-Neto PR, Jackson DA (2001) How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129:169–178.  https://doi.org/10.1007/s004420100720 CrossRefPubMedGoogle Scholar
  41. 41.
    De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684.  https://doi.org/10.1111/j.1600-0706.2010.18334.x CrossRefGoogle Scholar
  42. 42.
    Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590.  https://doi.org/10.1038/nrmicro.2017.87 CrossRefPubMedGoogle Scholar
  43. 43.
    Deshpande V, Wang Q, Greenfield P, Charleston M, Porras-Alfaro A, Kuske CR, Cole JR, Midgley DJ, Tran-Dinh N (2016) Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108:1–5.  https://doi.org/10.3852/14-293 CrossRefPubMedGoogle Scholar
  44. 44.
    Fernandez CW, Kennedy PG (2016) Revisiting the “Gadgil effect”: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394.  https://doi.org/10.1111/nph.13648 CrossRefPubMedGoogle Scholar
  45. 45.
    Trocha LK, Kałucka I, Stasińska M, Nowak W, Dabert M, Leski T, Rudawska M, Oleksyn J (2011) Ectomycorrhizal fungal communities of native and non-native Pinus and Quercus species in a common garden of 35-year-old trees. Mycorrhiza 22:121–134.  https://doi.org/10.1007/s00572-011-0387-x CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Pringle A, Vellinga EC (2006) Last chance to know? Using literature to explore the biogeography and invasion biology of the death cap mushroom Amanita phalloides (Vaill. Ex fr. : Fr.) link. Biol Invasions 8:1131–1144.  https://doi.org/10.1007/s10530-005-3804-2 CrossRefGoogle Scholar
  47. 47.
    Healy RA, Zurier H, Bonito G, Smith ME, Pfister DH (2016) Mycorrhizal detection of native and non-native truffles in a historic arboretum and the discovery of a new North American species, Tuber arnoldianum sp. nov. Mycorrhiza 26:781–792.  https://doi.org/10.1007/s00572-016-0713-4 CrossRefPubMedGoogle Scholar
  48. 48.
    Tedersoo L, Suvi T, Beaver K, Kõljalg U (2007) Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytol 175:321–333.  https://doi.org/10.1111/j.1469-8137.2007.02104.x CrossRefPubMedGoogle Scholar
  49. 49.
    Bonito G, Trappe JM, Donovan S, Vilgalys R (2011) The Asian black truffle Tuber indicum can form ectomycorrhizas with North American host plants and complete its life cycle in non-native soils. Fungal Ecol 4:83–93.  https://doi.org/10.1016/j.funeco.2010.08.003 CrossRefGoogle Scholar
  50. 50.
    Nuñez MA, Dickie IA (2014) Invasive belowground mutualists of woody plants. Biol Invasions 16:645–661.  https://doi.org/10.1007/s10530-013-0612-y CrossRefGoogle Scholar
  51. 51.
    Nikles DG (2006) The domestication of African mahogany (Khaya senegalensis) in northern Australia. Aust For 69:68–69.  https://doi.org/10.1080/00049158.2006.10674989 CrossRefGoogle Scholar
  52. 52.
    Norghauer JM, Martin AR, Mycroft EE, James A, Thomas SC (2011) Island invasion by a threatened tree species: evidence for natural enemy release of mahogany (Swietenia macrophylla) on Dominica, Lesser Antilles. PLoS One 6:e18790.  https://doi.org/10.1371/journal.pone.0018790 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Ibrahim D, Lee CC, Sheh-Hong L (2014) Antimicrobial activity of endophytic fungi isolated from Swietenia macrophylla leaves. Nat Prod Commun 9:247–250PubMedGoogle Scholar
  54. 54.
    Dewanjee S, Kundu M, Maiti A, Majumdar R, Majumdar A, Mandel SC (2007) In vitro evaluation of antimicrobial activity of crude extract from plants Diospyros peregrina, Coccinia grandis and Swietenia macrophylla. Trop J Pharm Res 6:773–778.  https://doi.org/10.4314/tjpr.v6i3.14658 CrossRefGoogle Scholar
  55. 55.
    Wang CJK, Wilcox HE (1985) New species of ectendomycorrhizal and pseudomycorrhizal fungi: Phialophora finlandia, Chloridium paucisporum, and Phialocephala fortinii. Mycologia 77:951–958.  https://doi.org/10.2307/3793308 CrossRefGoogle Scholar
  56. 56.
    Rodríguez-Morelos VH, Soto-Estrada A, Pérez-Moreno J, Franco-Ramírez A, Díaz-Rivera P (2014) Arbuscular mycorrhizal fungi associated with the rhizosphere of seedlings and mature trees of Swietenia macrophylla (Magnoliophyta: Meliaceae) in Los Tuxtlas, Veracruz, Mexico. Rev Chil Hist Nat. 87.  https://doi.org/10.1186/s40693-014-0009-z
  57. 57.
    de Souza RSC, Okura VK, Armanhi JSL et al (2016) Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci Rep 6:28774.  https://doi.org/10.1038/srep28774 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Bredeson JV, Lyons JB, Prochnik SE, Wu GA, Ha CM, Edsinger-Gonzales E, Grimwood J, Schmutz J, Rabbi IY, Egesi C, Nauluvula P, Lebot V, Ndunguru J, Mkamilo G, Bart RS, Setter TL, Gleadow RM, Kulakow P, Ferguson ME, Rounsley S, Rokhsar DS (2016) Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat Biotechnol 34:562–570.  https://doi.org/10.1038/nbt.3535 CrossRefPubMedGoogle Scholar
  59. 59.
    De Boer AJ, Chandra S (1978) A model of crop selection in semi-subsistence agriculture and an application to mixed agriculture in Fiji. Am J Agric Econ 60:436–444.  https://doi.org/10.2307/1239940 CrossRefGoogle Scholar
  60. 60.
    Straker CJ, Hilditch AJ, Rey MEC (2010) Arbuscular mycorrhizal fungi associated with cassava (Manihot esculenta Crantz) in South Africa. S Afr J Bot 76:102–111.  https://doi.org/10.1016/j.sajb.2009.09.005 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plants, Soil and Microbial SciencesMichigan State UniversityEast LansingUSA
  2. 2.Reef ExplorerNadrogaFiji Islands

Personalised recommendations