Advertisement

Coral Reefs

pp 1–10 | Cite as

Biodiversity of endolithic fungi in coral skeletons and other reef substrates revealed with 18S rDNA metabarcoding

  • Aristóteles Góes-Neto
  • Vanessa Rossetto Marcelino
  • Heroen Verbruggen
  • Felipe Ferreira da Silva
  • Fernanda BadottiEmail author
Report

Abstract

Corals live in close association with a diverse community of eukaryotes, bacteria, archaea and viruses that, together with the coral host, form the coral holobiont. Fungi are an important component of the coral holobiont; however, knowledge about their taxonomic diversity and the ecological functions these organisms play in reef corals is still scarce. In this study, we used metabarcoding to characterize the fungal community inhabiting the skeleton of eleven coral genera, as well as samples of crustose coralline algae, from Australia and Papua New Guinea. Most of the 24 distinct fungal genera identified were assigned to the phylum Ascomycota, followed by Basidiomycota. Lulworthia and Lulwoana (Ascomycota) were the most abundant and prevalent genera detected in our study. Besides these widely distributed genera, others never associated with corals or marine environments before, such as Geranomyces (Chytriomycota), Flammulina (Basidiomycota) and Ophiosphaerella (Ascomycota), were also detected. The predicted functional groups give insights into potential lifestyles and ecological functions of the fungal community in reef ecosystems. This study provides important observational data on a group of holobiont members that has received little attention.

Keywords

Fungal diversity Coral Reef substrates Metabarcoding Mycobiome Endolithic 

Notes

Acknowledgements

The authors would like to thank the Graduate Programs in Microbiology (http://www.microbiologia.icb.ufmg.br/pos/) and Bioinformatics (http://www.pgbioinfo.icb.ufmg.br). AG–N received a productivity research grant (no. 310764/2016-5) from the National Council for Scientific and Technological Development (http://www.cnpq.br). VRM is supported by the Sydney Medical School Foundation. This work was supported by the Australian Biological Resources Study (RFL213-08).

Authors Contributions

VRM and HV collected the samples and performed the amplifications and sequencing experiments. FB conceptualized the study and wrote the paper. FFS performed the bioinformatic analyses. AG–N supervised the analyses and contributed in all the steps of the study. All the authors contributed with the data analyses and with the manuscript written.

Compliance with ethical standards

Competing interests

The authors declare they have no conflict of interest.

Supplementary material

338_2019_1880_MOESM1_ESM.xlsx (19 kb)
Supplementary material 1 (XLSX 19 kb)
338_2019_1880_MOESM2_ESM.docx (19 kb)
Supplementary material 2 (DOCX 18 kb)

References

  1. Ainsworth T, Gates R (2016) Corals’ microbial sentinels. Science 352:1518–1519PubMedCrossRefGoogle Scholar
  2. Ainsworth T, Fordyce A, Camp E (2017) The other microeukaryotes of the coral reef microbiome. Trends Microbiol 25:980–991PubMedCrossRefGoogle Scholar
  3. Alker A, Smith G, Kim K (2001) Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiologia 460:105–111CrossRefGoogle Scholar
  4. Amend A (2014) From dandruff to deep-sea vents: malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog 10:e1004277PubMedPubMedCentralCrossRefGoogle Scholar
  5. Amend A, Barshis D, Oliver T (2011) Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J 6:1291–1301PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baker A, Correa A, Cunning R (2016) Diversity, distribution and stability of symbiodinium in reef corals of the eastern tropical pacific. In: Coral Reefs of the Eastern Tropical Pacific 405–420Google Scholar
  7. Bentis C, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order: Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260PubMedCrossRefGoogle Scholar
  8. Binder M, Hibbett D, Wang Z, Farnham W (2006) Evolutionary relationships of Mycaureola dilseae (Agaricales), a basidiomycete pathogen of a subtidal rhodophyte. Am J Bot 93:547–556PubMedCrossRefGoogle Scholar
  9. Bonthond G, Merselis D, Dougan K, Graff T, Todd W, Fourqurean J, Rodriguez-Lanetty M (2018) Inter-domain microbial diversity within the coral holobiont Siderastrea siderea from two depth habitats. Peer J 6:e4323PubMedCrossRefGoogle Scholar
  10. Bourne D, Webster N (2013) Coral reef bacterial communities. The Prokaryotes 163–187Google Scholar
  11. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden T (2009) BLAST + : architecture and applications. BMC Bioinformatics 10:421PubMedPubMedCentralCrossRefGoogle Scholar
  12. Clausen PT, Aarestrup FM, Lund O (2018) Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics 19(1):307PubMedPubMedCentralCrossRefGoogle Scholar
  13. Edgar R, Haas B, Clemente J, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200PubMedPubMedCentralCrossRefGoogle Scholar
  14. Egan S, Gardiner M (2016) Microbial dysbiosis: rethinking disease in marine ecosystems. Front Microbiol 7:991PubMedPubMedCentralGoogle Scholar
  15. Freiwald A, Reitner J, Krutschinna J (1997) Microbial alteration of the deep-water coral Lophelia pertusa: early postmortem processes. Facies 36:223–226Google Scholar
  16. Gaitanis G, Magiatis P, Hantschke M, Bassukas I, Velegraki A (2012) The malassezia genus in skin and systemic diseases. Clin Microbiol Rev 25:106–141PubMedPubMedCentralCrossRefGoogle Scholar
  17. Gleason F, Gadd G, Pitt J, Larkum A (2017) The roles of endolithic fungi in bioerosion and disease in marine ecosystems. II. Potential facultatively parasitic anamorphic ascomycetes can cause disease in corals and molluscs. Mycology 8:216–227PubMedPubMedCentralCrossRefGoogle Scholar
  18. Golubic S, Radtke G, Campion-Alsumard T (2005) Endolithic fungi in marine ecosystems. Trends Microbiol 13:229–235PubMedCrossRefGoogle Scholar
  19. Grossart HP, Rojas-Jimenez K (2016) Aquatic fungi: targeting the forgotten in microbial ecology. Curr Opin Microbiol 31:140–145PubMedCrossRefGoogle Scholar
  20. Grossart HP, Van den Wyngaert S, Kagami M, Wurzbacher C, Cunliffe M, Rojas-Jimenez K (2019) Fungi in aquatic ecosystems. Nat Rev Microbiol 17:339–354PubMedCrossRefGoogle Scholar
  21. Gullino M, Mocioni M, Titone P (2007) First report of ophiosphaerella korrae causing spring dead spot of Bermudagrass in Italy. Plant Dis 91:1200PubMedCrossRefGoogle Scholar
  22. Harvell D, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195CrossRefGoogle Scholar
  23. Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. The Fungal Kingdom 79–95Google Scholar
  24. Hoegh-Guldberg O, Mumby P, Hooten A, Steneck R, Greenfield P, Gomez E, Harvell C, Sale P, Edwards A, Caldeira K, Knowlton N, Eakin C, Iglesias-Prieto R, Muthiga N, Bradbury R, Dubi A, Hatziolos M (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  25. Jones E, Pang K (2012) Marine fungi and fungal-like organisms. De Gruyter, BostonCrossRefGoogle Scholar
  26. Jones E, Suetrong S, Sakayaroj J, Bahkali A, Abdel-Wahab M, Boekhout T, Pang K (2015) Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 73:1–72CrossRefGoogle Scholar
  27. Kendrick B, Risk MJ, Michaelides J, Bergman K (1982) Amphibious microborers: bioeroding fungi isolated from live corals. Deep sea research Part B. Oceanographic Lit Rev 30:469Google Scholar
  28. Kirk P, Cannon P, Minter D, Stalpers J (2013) Dictionary of the fungi. CABI Publishing, WallingfordGoogle Scholar
  29. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62PubMedCrossRefGoogle Scholar
  30. Kohlmeyer J (1969) The role of marine fungi in the penetration of calcareous substances. Am Zool 9:741–746CrossRefGoogle Scholar
  31. Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic Press, New YorkGoogle Scholar
  32. Kohlmeyer J, Spatafora J, Volkmann-Kohlmeyer B (2000) Lulworthiales, a new order of marine ascomycota. Mycologia 92:453CrossRefGoogle Scholar
  33. Lesser M, Stat M, Gates R (2013) The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32:603–611CrossRefGoogle Scholar
  34. Littman R, Willis Bourne D (2011) Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Reports 3:651–660CrossRefGoogle Scholar
  35. Marcelino VR, Verbruggen H (2016) Multi-marker metabarcoding of coral skeletons reveals a rich microbiome and diverse evolutionary origins of endolithic algae. Sci Rep 6:31508PubMedPubMedCentralCrossRefGoogle Scholar
  36. Marcelino VR, van Oppen M, Verbruggen H (2017) Highly structured prokaryote communities exist within the skeleton of coral colonies. ISME J 12:300–303PubMedPubMedCentralCrossRefGoogle Scholar
  37. Marcelino VR, Clausen PT, Buchman J, Wille M, Iredell JR, Meyer W, Lund O, Sorrell T, Holmes EC (2019) CCMetagen: comprehensive and accurate identification of eukaryotes and prokaryotes in metagenomic data. BioRxiv 1:641332Google Scholar
  38. Nguyen N, Song Z, Bates S, Branco S, Tedersoo L, Menke J, Schilling J, Kennedy P (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20:241–248CrossRefGoogle Scholar
  39. Nieves-Rivera A (2015) Coastal mycology of Puerto Rico. Lulu Press, MorrisvilleGoogle Scholar
  40. Peters EC (2015) Diseases of coral reef organisms. In: Birkeland C (ed) Coral reefs in the anthropocene. Springer, DordrechtGoogle Scholar
  41. Porazinska DL, Giblin-Davis RM, Faller L, Farmerie W, Kanzaki N, Morris K, Thomas WK (2009) Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Mol Ecol Resour 9(6):1439–1450PubMedCrossRefGoogle Scholar
  42. Priess K, Le Campion-Alsumard T, Golubic S, Gadel F, Thomassin B (2000) Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton. Mar Biol 136:19–27CrossRefGoogle Scholar
  43. Raghukumar S (2017) Fungi in coastal and oceanic marine ecosystems. Springer, BerlinCrossRefGoogle Scholar
  44. Raghukumar, C, Ravindran J (2012) Fungi and their role in corals and coral reef ecosystems. In: Biology of marine fungi. Springer, Berlin, Heidelberg, pp 89–113Google Scholar
  45. Ravindran J, Raghukumar C, Raghukumar S (2001) Fungi in Porites lutea: association with healthy and diseased corals. Dis Aquat Organ 47:219–228PubMedCrossRefGoogle Scholar
  46. Richards T, Jones M, Leonard G, Bass D (2012) Marine fungi: their ecology and molecular diversity. Ann Rev Mar Sci 4:495–522PubMedCrossRefGoogle Scholar
  47. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. Peer J 4:e2584PubMedCrossRefGoogle Scholar
  48. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  49. Simmons DR (2011) Phylogeny of Powellomycetaceae fam. nov. and description of Geranomyces variabilis gen. et comb. nov. Mycologia 103(6):1411–1420.  https://doi.org/10.3852/11-039 CrossRefPubMedGoogle Scholar
  50. Soler-Hurtado M, Sandoval-Sierra J, Machordom A, Diéguez-Uribeondo J (2016) Aspergillus sydowii and other potential fungal pathogens in gorgonian octocorals of the ecuadorian pacific. PLOS ONE 11:e0165992PubMedPubMedCentralCrossRefGoogle Scholar
  51. Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11(8):2148–2163CrossRefGoogle Scholar
  52. Toledo-Hernández C, Zuluaga-Montero A, Bones-González A, Rodríguez J, Sabat A, Bayman P (2008) Fungi in healthy and diseased sea fans (Gorgonia ventalina): is Aspergillus sydowii always the pathogen? Coral Reefs 27:707–714CrossRefGoogle Scholar
  53. Tribollet A, Payri C (2001) Bioerosion of the coralline alga Hydrolithon onkodes by microborers in the coral reefs of Moorea, French Polynesia. Oceanol Acta 24:329–342CrossRefGoogle Scholar
  54. Wang Y, Guo X, Zheng P, Zou S, Li G, Gong J (2017) Distinct seasonality of chytrid-dominated benthic fungal communities in the neritic oceans (Bohai Sea and North Yellow Sea). Fungal Ecol 30:55–66CrossRefGoogle Scholar
  55. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719PubMedCrossRefGoogle Scholar
  56. Xu W, Guo S, Gong L, Alias SA, Pang KL, Luo ZH (2018) Phylogenetic survey and antimicrobial activity of cultivable fungi associated with five scleractinian coral species in the South China Sea. Botanica marina 61(1):75–84CrossRefGoogle Scholar
  57. Yarden O (2014) Fungal association with sessile marine invertebrates. Front Microbiol 5:228PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Microbiology, Institute of Biological SciencesUniversidade Federal de Minas Gerais (UFMG)Belo HorizonteBrazil
  2. 2.School of BiosciencesUniversity of MelbourneParkvilleAustralia
  3. 3.Marie Bashir Institute for Infectious Diseases and Biosecurity and Sydney Medical SchoolUniversity of SydneySydneyAustralia
  4. 4.Department of ChemistryCentro Federal de Educação Tecnológica de Minas Gerais (CEFET-MG)Belo HorizonteBrazil

Personalised recommendations