Abstract
Aims
Arbuscular mycorrhizal (AM) fungi often occur in mangrove ecosystems, but how different AM fungi interact with mangrove plants is still unclear. Here, we aimed to study the root colonization patterns of AM fungi in two major mangrove tree species, Rhizophora stylosa Griff. and Bruguiera gymnorhiza (L.) Lam., that dominate the estuarine and freshwater sides of an ecotone.
Methods
We sampled the roots and soils in a mangrove forest on an island in southern Japan and examined the root colonization rates and community compositions of AM fungi using microscopy and high-throughput sequencing of the small subunit (18S) rRNA gene.
Results
Microscopy revealed AM fungal structures in roots from some individuals of B. gymnorhiza but not of R. stylosa. Molecular analysis detected DNA sequences of Glomeraceae species in roots of both species, but detected those of Acaulosporaceae species only in B. gymnorhiza roots. Glomeraceae species were associated with higher soil electrical conductivity (EC), and Acaulosporaceae species with lower soil EC. The presence/absence of sequences of Acaulosporaceae species was significantly associated with the presence/absence of AM fungal structures (microscopic evidence) in B. gymnorhiza.
Conclusions
Our results suggest that salinity influences AM fungal community composition in mangrove soils, and that AM fungi such as Acaulosporaceae species form trophic associations with B. gymnorhiza and could help mangrove tree nutrition in saline and low-nutrient environments.
Similar content being viewed by others
Data availability
The sequence data has been deposited in the DNA Data Bank of Japan (DDBJ) sequence read archive (accession number DRA010799). The other data are available in the electronic supplementary material.
Code availability
Not applicable.
Change history
28 May 2022
A Correction to this paper has been published: https://doi.org/10.1007/s11104-022-05454-w
References
Ahlmann-Eltze C (2019) ggsignif: significance brackets for ‘ggplot2’, R package version 0.6.0. https://CRAN.R-project.org/package=ggsignif
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Becker RA, Wilks AR, Brownrigg R, Minka TP, Deckmyn A (2018) maps: draw geographical maps, R package version 3.3.0. https://CRAN.R-project.org/package=maps
Bivand RS, Wong DWS (2018) Comparing implementations of global and local indicators of spatial association. TEST 27:716–748. https://doi.org/10.1007/s11749-018-0599-x
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:33–77. https://doi.org/10.1007/s11104-008-9877-9
Brundrett MC, Tedersoo L (2020) Resolving the mycorrhizal status of important northern hemisphere trees. Plant Soil 454:3–34. https://doi.org/10.1007/s11104-020-04627-9
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Changnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. https://doi.org/10.1016/j.tplants.2013.05.001
Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547. https://doi.org/10.1890/11-1952.1
Chen E, Blaze JA, Smith RS, Peng S, Byers JE (2020) Freeze tolerance of poleward-spreading mangrove species weakened by soil properties of resident salt marsh competitor. J Ecol 108:1725–1737. https://doi.org/10.1111/1365-2745.13350
Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196:483–493. https://doi.org/10.1016/j.ecolmodel.2006.02.015
Dray S, Bauman D, Blanchet G, Borcard D, Clappe S, Guenard G, Jombart T, Larocque G, Legendre P, Madi N, Wagner HH (2019) adespatial: multivariate multiscale spatial analysis, R package version 0.3-7. https://CRAN.R-project.org/package=adespatial
D’Souza J, Rodrigues BF (2013) Biodiversity of Arbuscular Mycorrhizal (AM) fungi in mangroves of Goa in West India. J Forestry Res 24:515–523. https://doi.org/10.1007/s11676-013-0342-0
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280. https://doi.org/10.1093/aob/mcp251
Fernández I, Cosme M, Stringlis IA, Yu K, de Jonge R, van Wees SCM, Pozo MJ, Pieterse CMJ, van der Heijden MGA (2019) Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism. New Phytol 223:867–881. https://doi.org/10.1111/nph.15798
Gallic E (2016) legendMap: north arrow and scale bar for ggplot2 graphics, R package version 1.0. https://github.com/3wen/legendMap
Gaonkar S, Rodrigues BF (2020) Diversity of arbuscular mycorrhizal (AM) fungi in mangroves of Chorao Island, Goa, India. Wetl Ecol Manag 28:765–778. https://doi.org/10.1007/s11273-020-09747-8
Gupta N, Bihari KM, Sengupta I (2016) Diversity of arbuscular mycorrhizal fungi in different salinity of mangrove ecosystem of Odisha, India. Adv Plants Agric Res 3:19–23. https://doi.org/10.15406/apar.2016.03.00085
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344. https://doi.org/10.1046/j.0028-646X.2001.00312.x
Inoue T, Kohzu A, Shimono A (2019) Tracking the route of atmospheric nitrogen to diazotrophs colonizing buried mangrove roots. Tree Physiol 39:1896–1906. https://doi.org/10.1093/treephys/tpz088
Inoue T, Shimono A, Akaji Y, Baba S, Takenaka A, Chan HT (2020) Mangrove–diazotroph relationships at the root, tree and forest scales: diazotrophic communities create high soil nitrogenase activities in Rhizophora stylosa rhizospheres. Ann Bot 125:131–144. https://doi.org/10.1093/aob/mcz164
Juniper S, Abbott L (1993) Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 4:45–57. https://doi.org/10.1007/BF00204058
Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379. https://doi.org/10.1007/s00572-006-0046-9
Kadoya T, Inoue T (2015) Spatio-temporal pattern of specific gravity of mangrove diaspore: implications for upstream dispersal. Ecography 38:472–479. https://doi.org/10.1111/ecog.01074
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436
Kothamasi D, Kothamasi S, Bhattacharyya A, Kuhad RC, Babu CR (2006) Arbuscular mycorrhizae and phosphate solubilising bacteria of the rhizosphere of the mangrove ecosystem of Great Nicobar island, India. Biol Fert Soils 42:358–361. https://doi.org/10.1007/s00374-005-0035-8
Krishnamoorthy R, Kim K, Kim C, Sa T (2014) Changes of arbuscular mycorrhizal traits and community structure with respect to soil salinity in a coastal reclamation land. Soil Biol Biochem 72:1–10. https://doi.org/10.1016/j.soilbio.2014.01.017
Kumar T, Ghose M (2008) Status of arbuscular mycorrhizal fungi (AMF) in the Sundarbans of India in relation to tidal inundation and chemical properties of soil. Wetl Ecol Manag 16:471–483. https://doi.org/10.1007/s11273-008-9085-7
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Lee BKH, Baker GE (1973) Fungi associated with the roots of red mangrove, Rhizophora mangle. Mycologia 65:894–906. https://doi.org/10.2307/3758522
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. https://doi.org/10.1111/j.1574-6941.2008.00531.x
Lovelock CE, Feller IC, Mckee KL, Engelbrecht BMJ, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panamá. Funct Ecol 18:25–33. https://doi.org/10.1046/j.0269-8463.2004.00805.x
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Lozupone CA, Knight R (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev 32:557–578. https://doi.org/10.1111/j.1574-6976.2008.00111.x
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
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
Mohankumar V, Mahadevan A (1986) Survey of vesicular-arbuscular mycorrhizae in mangrove vegetation. Curr Sci 55:936
Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411. https://doi.org/10.1016/S0169-5347(00)89157-0
Nielsen KB, Kjøller R, Olsson PA, Schweiger PF, Andersen FØ, Rosendahl S (2004) Colonisation and molecular diversity of arbuscular mycorrhizal fungi in the aquatic plants Littorella uniflora and Lobelia dortmanna in southern Sweden. Mycol Res 108:616–625. https://doi.org/10.1017/S0953756204000073
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: community ecology package, R package version 2.5-6. https://CRAN.R-project.org/package=vegan
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. https://doi.org/10.1111/j.1469-8137.2010.03334.x
Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Pebesma E (2018) Simple features for R: standardized support for spatial vector data. R J 10:439–446. https://doi.org/10.32614/RJ-2018-009
R Core Team (2019) R: a language and environment for statistical computing. R Foundation, Vienna
Ramírez-Viga T, Guadarrama P, Castillo-Argüero S, Estrada-Medina H, García-Sánchez R, Hernández-Cuevas L, Sánchez-Gallén I, Ramos-Zapata J (2020) Relationship between arbuscular mycorrhizal association and edaphic variables in mangroves of the coast of Yucatán, Mexico. Wetlands 40:539–549. https://doi.org/10.1007/s13157-019-01196-1
Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30:1148–1160. https://doi.org/10.1093/treephys/tpq048
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million‐year‐old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci 91:11841–11843. https://doi.org/10.1073/pnas.91.25.11841
Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 342:459–468. https://doi.org/10.1007/s11104-010-0709-3
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl Sci 51:179–181. https://doi.org/10.1111/j.1744-697X.2005.00023.x
Sengupta A, Chaudhuri S (2002) Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174. https://doi.org/10.1007/s00572-002-0164-y
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, third. Academic, New York
Spalding M, Kainuma M, Collins L (2010) World Atlas of Mangroves. Earthscan Ltd., London
Teste FP, Jones MD, Dickie IA (2020) Dual-mycorrhizal plants: their ecology and relevance. New Phytol 225:1835–1851. https://doi.org/10.1111/nph.16190
Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, Cambridge
Tommerup IC, Abbott LK (1981) Prolonged survival and viability of VA mycorrhizal hyphae after root death. Soil Biol Biochem 13:431–433. https://doi.org/10.1016/0038-0717(81)90090-0
Wang Y, Qiu Q, Yang Z, Hu Z, Tam NFY, Xin G (2010) Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 331:181–191. https://doi.org/10.1007/s11104-009-0244-2
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. https://doi.org/10.1371/journal.pone.0024512
Wang Y, Qiu Q, Li S, Xin G, Tam NFY (2014) Inhibitory effect of municipal sewage on symbiosis between mangrove plants and arbuscular mycorrhizal fungi. Aquat Biol 20:119–127. https://doi.org/10.3354/ab00550
Wang Y, Li T, Li Y, Qiu Q, Li S, Xin G (2015) Distribution of arbuscular mycorrhizal fungi in four semi-mangrove plant communities. Ann Microbiol 65:603–610. https://doi.org/10.1007/s13213-014-0896-x
Wang Y, Li Y, Bao X, Björn LO, Li S, Olsson PA (2016) Response differences of arbuscular mycorrhizal fungi communities in the roots of an aquatic and a semiaquatic species to various flooding regimes. Plant Soil 403:361–373. https://doi.org/10.1007/s11104-016-2811-7
Wang Y, Li Y, Li S, Rosendahl S (2021) Ignored diversity of arbuscular mycorrhizal fungi in co-occurring mycotrophic and non-mycotrophic plants. Mycorrhiza 31:93–102. https://doi.org/10.1007/s00572-020-00997-1
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
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. https://doi.org/10.1111/j.1462-2920.2009.01882.x
Yu G, Smith D, Zhu H, Guan Y, Lam TTY (2017) ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36. https://doi.org/10.1111/2041-210X.12628
Zhao ZW, Xia YM, Qin XZ, Li XW, Cheng LZ, Sha T, Wang GH (2001) Arbuscular mycorrhizal status of plants and the spore density of arbuscular mycorrhizal fungi in the tropical rain forest of Xishuangbanna, southwest China. Mycorrhiza 11:159–162. https://doi.org/10.1007/s005720100117
Acknowledgements
We thank Mr. K. Kaneko and the staff at Iriomote Station, Tropical Biosphere Research Center, University of the Ryukyus for their assistance with the field survey. The comments of anonymous reviewers improved this manuscript substantially. This work was funded by the Joint Research Program of Arid Land Research Center, Tottori University (grant no. 30D2002) and the Environment Research and Technology Development Fund (project nos. JPMEERF20172012, JPMEERF15S11400) of the Environmental Restoration and Conservation Agency of Japan.
Funding
This work was funded by the Joint Research Program of Arid Land Research Center, Tottori University (grant no. 30D2002) and the Environment Research and Technology Development Fund (project nos. JPMEERF20172012, JPMEERF15S11400) of the Environmental Restoration and Conservation Agency of Japan.
Author information
Authors and Affiliations
Contributions
Y.A. and T.I. conceived the research; Y.A., T.I., and S.B. conducted the field survey and sampling; Y.A. and T.T. conducted the molecular experiments and data analysis; Y.A. wrote the draft; all authors contributed to the drafts and approved publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Additional information
Responsible Editor: François Teste.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Akaji, Y., Inoue, T., Taniguchi, T. et al. Arbuscular mycorrhizal fungal communities of a mangrove forest along a salinity gradient on Iriomote Island. Plant Soil 472, 145–159 (2022). https://doi.org/10.1007/s11104-021-05193-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05193-4