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Phylogenetic Diversity of Sponge-Associated Fungi from the Caribbean and the Pacific of Panama and Their In Vitro Effect on Angiotensin and Endothelin Receptors

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Abstract

Fungi occupy an important ecological niche in the marine environment, and marine fungi possess an immense biotechnological potential. This study documents the fungal diversity associated with 39 species of sponges and determines their potential to produce secondary metabolites capable of interacting with mammalian G-protein-coupled receptors involved in blood pressure regulation. Total genomic DNA was extracted from 563 representative fungal strains obtained from marine sponges collected by SCUBA from the Caribbean and the Pacific regions of Panama. A total of 194 operational taxonomic units were found with 58 % represented by singletons based on the internal transcribed spacer (ITS) and partial large subunit (LSU) rDNA regions. Marine sponges were highly dominated by Ascomycota fungi (95.6 %) and represented by two major classes, Sordariomycetes and Dothideomycetes. Rarefaction curves showed no saturation, indicating that further efforts are needed to reveal the entire diversity at this site. Several unique clades were found during phylogenetic analysis with the highest diversity of unique clades in the order Pleosporales. From the 65 cultures tested to determine their in vitro effect on angiotensin and endothelin receptors, the extracts of Fusarium sp. and Phoma sp. blocked the activation of these receptors by more than 50 % of the control and seven others inhibited between 30 and 45 %. Our results indicate that marine sponges from Panama are a “hot spot” of fungal diversity as well as a rich resource for capturing, cataloguing, and assessing the pharmacological potential of substances present in previously undiscovered fungi associated with marine sponges.

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Acknowledgments

The authors thank the National Secretariat of Science and Technology of the Republic of Panama for financial support by grants of international collaboration number COL08-014 and COL10-070 and by a partnership program between the Organization for the Prohibition of Chemical Weapons (The Hague, Netherlands) and the International Foundation for Science (Stockholm, Sweden). The College of Agriculture and Life Sciences at The University of Arizona is gratefully acknowledge for technical and logistical support for molecular analyses, Prof. Dr. Luis D’Croz for critically reviewing this work, Juan B. Del Rosario for research assistance, and the Smithsonian Tropical Research Institute for laboratory facilities, boats, and technical support. The authors also want to thank the Panamanian Authority of the Environment (ANAM) for their collaboration.

Conflict of Interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Institute of Scientific Research and High Technology Services, Bld. 219, City of Knowledge, Clayton, Panama, Republic of Panama

    Jessica Bolaños, Luis Fernando De León & Catherina Caballero-George

  2. Conservation International, 2011 Crystal Dr. Suite 500, 22202, Arlington, VA, USA

    Edgardo Ochoa

  3. Instituto de Productos Naturales y Agrobiología (IPNA), Consejo Superior de Investigaciones Científicas, Avda. Astrofísico Fco. Sánchez, 3, 38206, La Laguna, Tenerife, Spain

    José Darias

  4. Department of Chemistry and Biochemistry, The University of North Carolina at Greensboro, 435 Sullivan Science Building, 301 McIver Street, Greensboro, NC, 27412, USA

    Huzefa A. Raja

  5. Department of Plant Biology, University of Illinois, 505 South Goodwin Avenue, Urbana, IL, 61801, USA

    Carol A. Shearer

  6. Illinois Natural History Survey, University of Illinois, 1816 South Oak Street, Champaign, IL, 61820, USA

    Andrew N. Miller

  7. Faculty of Sciences and Bioengineering Sciences, Vrije Universiteit Brussel, Building E, Room E7.09, Pleinlaan 2, B-1050, Brussels, Belgium

    Patrick Vanderheyden

  8. Department of Biological Sciences, Western Illinois University, Waggoner Hall 372, 1 University Circle, Macomb, IL, 61455, USA

    Andrea Porras-Alfaro

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  1. Jessica Bolaños
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  2. Luis Fernando De León
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Correspondence to Catherina Caballero-George.

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Online Resource 1

Rarefaction curves indicating the overall number of culturable fungal species found in three geographical regions (top panel) and isolated from multiple sponge orders (lower panel) as a function of sampling effort. Sponge orders shown in this figure represent the most common or the most sampled sponges. In both cases, there is no clear evidence for saturation in the number of species. (GIF 51 kb)

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Appendices

Appendices

Appendix 1

Table 4 Affiliation of the fungal isolates from sponges collected in the Republic of Panama
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Appendix 2

Table 5 Number of fungi isolated and sequenced per sponge specimen
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Appendix 3

Table 6 Percentage of receptor inhibition by 100 μg/ml fungal extracts. Data represents the average and the standard deviation of three independent experiments
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Bolaños, J., De León, L.F., Ochoa, E. et al. Phylogenetic Diversity of Sponge-Associated Fungi from the Caribbean and the Pacific of Panama and Their In Vitro Effect on Angiotensin and Endothelin Receptors. Mar Biotechnol 17, 533–564 (2015). https://doi.org/10.1007/s10126-015-9634-z

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