Advertisement

Fungal Diversity

, Volume 42, Issue 1, pp 17–26 | Cite as

Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge

  • Z. Paz
  • M. Komon-Zelazowska
  • I. S. Druzhinina
  • M. M. Aveskamp
  • A. Shnaiderman
  • Y. Aluma
  • S. Carmeli
  • M. Ilan
  • O. YardenEmail author
Article

Abstract

Fungi that inhabit marine sponges occupy an ecological niche that has recently attracted great attention due to the potential in either ecological or pharmaceutical advances. The ecological interaction between marine sponges and fungi is, however, only poorly understood. Eighty five fungal taxa were isolated from the marine sponge Psammocinia sp. from the Mediterranean Sea. The majority (89%) of these taxa were isolated using a `sample compressing` method, in combination with the use of fungicides-amended medium. Abundant `terrestrial` taxa such as Acremonium, Penicillium and Trichoderma were found along with potentially undescribed Phoma and Trichoderma species. Several of these taxa exhibited in vitro anti-fungal properties as determined against four test fungi. Even though a significant number of fungal taxa were isolated during this study, we estimate that the diversity of fungi that are associated with Psammocinia sp. is higher than reported here. It is advocated that Psammocinia, and other sponge genera, may be a prime niche for discovering new fungal species as well as novel anti-fungal compounds from fungal sources.

Keywords

Acremonium Aspergillus Fungicides Marine fungi Penicillium Phoma Psammocinia Trichoderma 

Notes

Acknowledgements

We thank Keith Seifert for his comments and advice on identification of Penicillium sp, Bente Kopeliovitch for technical assistance and R. Hefetz from Makhteshim- Agan Industries Ltd. for providing the fungicides used for this study. This study was supported by the Israel Science Foundation (ISF 996/06).

References

  1. Barghoorn ES, Linder DH (1944) Marine fungi: their taxonomy and biology. Farlowia 1:395–467Google Scholar
  2. Bergquist PR (1978) Sponges. University of California Press, Berkeley, pp 181–185Google Scholar
  3. Bhadury P, Mohammad BT, Wright PC (2006) The current status of natural products from marine fungi and their potential as anti-infective agents. J Ind Microbiol Biotechnol 33:325–337CrossRefPubMedGoogle Scholar
  4. Bridge PD (2002) The history and application of molecular mycology. Mycologist 16:90–99CrossRefGoogle Scholar
  5. Bugni TS, Ireland CM (2004) Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 21:143–163CrossRefPubMedGoogle Scholar
  6. Druzhinina IS, Kopchinskiy AG, Komoń M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813–828CrossRefPubMedGoogle Scholar
  7. Druzhinina IS, Komoń-Zelazowska M, Kredics L, Hatvani L, Antal Z, Belayneh T, Kubicek CP (2008) Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable to cause invasive mycoses of humans. Microbiology SGM 154:3447–3459CrossRefGoogle Scholar
  8. Duong LM, Jeewon R, Lumyong S, Hyde KD (2006) DGGE coupled with ribosomal DNA gene phylogenies reveal uncharacterized fungal phylotypes. Fungal Divers 23:121–138Google Scholar
  9. Ein-Gil N, Ilan M, Carmeli S, Smith GW, Pawlik JR, Yarden O (2009) Presence of Aspergillus sydowii, a pathogen of gorgonian sea-fans in the marine sponge Spongia obscura. The ISME Journal 3:752–755Google Scholar
  10. Gao Z, Li B, Chengchao Z, Wang G (2008) Molecular detection of fungal communities in the Hawaiian marine sponges Suberites zeteki and Mycale armata. Appl Environ Microbiol 74:6091–6101CrossRefPubMedGoogle Scholar
  11. Geiser DM, Taylor JW, Ritchie KB, Smith GW (1998) Cause of sea-fan death in the West Indies. Nature 394:137–138CrossRefGoogle Scholar
  12. Geiser DM, del Mar Jiménez-Gasco M, Kang SC, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) FUSARIUM-ID v; 1;0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479CrossRefGoogle Scholar
  13. Gomez-Guinan Y, Hidalgo J, Jimenez M, Salcedo J (2003) Organic extracts with antimicrobian activity from Penicillium sp (Moniliales) isolated from the sponge ircinia felix (Porifera: Demospongiae). Rev Biol Trop 51:141–147PubMedGoogle Scholar
  14. Guo LD, Hyde KD, Liew ECY (2001) Detection and taxonomic placement of endophytic fungi within frond tissues of Livistona chinensis based on rDNA sequences. Mol Phylogenet Evol 19:1–13CrossRefGoogle Scholar
  15. Guo LD, Huang GR, Wang Y, He WH, Zheng WH, Hyde KD (2003) Molecular identification of white morphotype strains of endophytic fungi from Pinus tabulaeformis. Mycol Res 107:680–688CrossRefPubMedGoogle Scholar
  16. Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134CrossRefGoogle Scholar
  17. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Müller WEG (ed) Molecular marine biology of sponges. Springer-Verlag, Heidelberg, pp 60–88Google Scholar
  18. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177CrossRefPubMedGoogle Scholar
  19. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192Google Scholar
  20. Höller H, Wright AD, Matthhee GF, Konig G, Draeger MS, Aust HJ, Schulz B (2000) Fungi from marine sponges: diversity, biological activity and secondary metabolites. Mycol Res 104:1354–1365CrossRefGoogle Scholar
  21. Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61–75Google Scholar
  22. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  23. Hyde KD, Jones EBG, Leano E, Pointing SB, Poonyth AD, Vrijmoed LLP (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161CrossRefGoogle Scholar
  24. Hyde KD, Sarma VV, Jones EBG (2000) Morphology and taxonomy of higher marine fungi. In: Hyde KD, Pointing SB (eds) Marine mycology: a practical approach. Fungal Diversity Press, The University of Hong Kong, Hong Kong, pp 172–204Google Scholar
  25. Jones EBG, Sakayaroj J, Suetrong S, Somrithipol S, Pang KL (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:1–187Google Scholar
  26. Kemp PF, Aller JY (2004) Estimating prokaryotic diversity: when 16s rDNA libraries large enough? Limnol Oceanogr: Methods 2:114–125Google Scholar
  27. Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic Press, New YorkGoogle Scholar
  28. Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of enduphytic fungi from Tripterygium wilfordii. Fungal Divers 17:69–90Google Scholar
  29. Lopanik N, Lindquist N, Targett N (2004) Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia 139:131–139CrossRefPubMedGoogle Scholar
  30. Maldonado M, Young CM (1998) Limits of the bathymetric distribution of keratose sponges: a field test in deep water. Mar Ecol Prog Ser 174:123–139CrossRefGoogle Scholar
  31. Mitchell AM, Strobel GA, Hess WM, Vargas PN, Ezra D (2008) Muscodor crispans, a novel endophyte from Ananas ananassoides in the Bolivian Amazon. Fungal Divers 31:37–43Google Scholar
  32. Morrison-Gardiner S (2002) Dominant fungi from Australian reefs. Fungal Divers 9:105–121Google Scholar
  33. Morton DJ, Stroube WH (1955) Antagonistic and stimulatory effects of soil microorganisms upon Sclerotium rolfsii. Phytopathology 45:417–420Google Scholar
  34. Paz Z, Burdman S, Gerson U, Sztejnberg A (2007) Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora. J Appl Microbiol 103:2570–2579CrossRefPubMedGoogle Scholar
  35. Proksch P, Ebel R, Edrada R, Riebe F, Liu H, Diesel A, Bayer M, Li X, Lin WH, Grebenyuk V, Mueller WEG, Draeger S, Zuccaro AA, Schulz B (2008) Sponge-associated fungi and their bioactive compounds: the Suberites case. Bot Mar 51:209–218CrossRefGoogle Scholar
  36. Raghukumar C (2008) Marine fungal biotechnology: an ecological perspective. Fungal Divers 31:19–35Google Scholar
  37. Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones EBG (2008) Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oil palm, Elaeis guineensis, in Thailand. Fungal Divers 33:139–162Google Scholar
  38. Samson RA, Seifert KA, Kuijpers AFA, Houbraken JAMP, Frisvad JC (2004) Phylogenetic analysis of Penicillium subgenus Penicillium using partial β-tubulin sequences. Stud Mycol 49:175–200Google Scholar
  39. Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87–100Google Scholar
  40. Seena S, Wynberg N, Bärlocher F (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Divers 30:1–14Google Scholar
  41. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  42. Tao G, Liu ZY, Hyde KD, Lui XZ, Yu ZN (2008) Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers 33:101–122Google Scholar
  43. Taylor MW, Schupp PJ, Kjelleberg DS, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130CrossRefPubMedGoogle Scholar
  44. Taylor MW, Hill RT, Piel J, Thacker RW, Hentschel U (2007a) Soaking it up: the complex lives of marine sponges and their microbial associates. ISME J 1:187–190CrossRefPubMedGoogle Scholar
  45. Taylor MW, Radax R, Steger D, Wagner M (2007b) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347CrossRefPubMedGoogle Scholar
  46. Thakur NL, Anil AC, Muller WEG (2004) Culturable epibacteria of the marine sponge Ircinia fusca: temporal variations and their possible role in the epibacterial defense of the host. Aquat Microb Ecol 37:295–304CrossRefGoogle Scholar
  47. Tsoukatou M, Hellio C, Vagias C, Harvala C, Roussis V (2002) Chemical defense and antifouling activity of three Mediterranean sponges of the genus Ircinia. Z Naturforsch 57:161–171Google Scholar
  48. Vijaykrishna D, Jeewon R, Hyde KD (2006) Molecular taxonomy, origins and evolution of freshwater ascomycetes. Fungal Divers 23:351–390Google Scholar
  49. Wang G (2006) Diversity and biotechnological potential of the sponge-associated microbial consortia. J Ind Microbiol Biotech 33:545–551CrossRefGoogle Scholar
  50. Wang Y, Guo LD, Hyde KD (2005) Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in northeast China based on rDNA sequences. Fungal Divers 20:235–260Google Scholar
  51. Wang G, Li Q, Zhu P (2008) Phylogenetic diversity of culturable fungi associated with the Hawaiian sponges Suberites zeteki and Gelliodes fibrosa. Antonie van Leeuwenhoek 93:163–174CrossRefPubMedGoogle Scholar
  52. Weisz JB, Hentschel U, Lindquist N, Martens CS (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol 152:475–483CrossRefGoogle Scholar
  53. Weisz JB, Lindquist N, Martens CS (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155:367–376CrossRefPubMedGoogle Scholar
  54. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gellfand DH, Sninisky JJ, White TJ (eds) PCR protocol: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  55. Wirsel SGR, Runge-Froböse C, Ahrén DG, Kemen E, Oliver RP, Mendgen KW (2002) Four or more species of Cladosporium sympatrically colonize Phragmites australis. Fungal Genet Biol 35:99–113CrossRefPubMedGoogle Scholar

Copyright information

© Kevin D Hyde 2010

Authors and Affiliations

  • Z. Paz
    • 1
  • M. Komon-Zelazowska
    • 2
  • I. S. Druzhinina
    • 2
  • M. M. Aveskamp
    • 3
  • A. Shnaiderman
    • 1
  • Y. Aluma
    • 4
  • S. Carmeli
    • 5
  • M. Ilan
    • 4
  • O. Yarden
    • 1
    Email author
  1. 1.Department of Plant Pathology and Microbiology, The R.H. Smith Faculty of Agriculture, Food and EnvironmentThe Hebrew University of JerusalemRehovotIsrael
  2. 2.Research Area of Gene Technology and Applied Biochemistry, Institute of Chemical EngineeringVienna University of TechnologyViennaAustria
  3. 3.CBS Fungal Biodiversity CentreUtrechtThe Netherlands
  4. 4.Department of Zoology, George S. Wise Faculty of Life SciencesTel Aviv UniversityRamat AvivIsrael
  5. 5.School of Chemistry, Raymond and Beverly Sackler Faculty of Exact SciencesTel Aviv UniversityRamat AvivIsrael

Personalised recommendations