Abstract
Marine sponges harbor numerous microorganisms, among which sponge-associated yeasts are the least explored. To gain greater knowledge of sponge-associated yeasts, an investigation was therefore performed on marine sponges in Sattahip Bay, Gulf of Thailand, South China Sea. Seventy-one (71) marine sponge samples were collected at sites near Samae-san, Mu, and Khram islands, and were subsequently identified as 17 sponge species in 14 genera. Eighty-seven (87) yeast strains were isolated from 42 samples. The identification of yeasts by similarity analysis of the D1/D2 domain sequences of the large subunit rRNA gene revealed that 64% of the yeast strains obtained belonged to the phylum Basidiomycota, while the remaining strains belonged to the phylum Ascomycota. The strains that belonged to Ascomycota comprised 11 known yeast species in five genera (Candida, Kodamaea, Magnusiomyces, Meyerozyma, and Pichia). The strains belonging to the phylum Basidiomycota comprised 14 known yeast species in eight genera (Cutaneotrichosporon, Cystobasidium, Naganishia, Papiliotrema, Rhodosporidiobolus, Rhodotorula, Trichosporon, and Vishniacozyma). In addition, three strains represented a potential novel species closest to Cys. slooffiae; one strain represented a potential novel species closest to R. toruloides; and one strain represented a potential novel species closest to V. foliicola. The species with the highest occurrence was Rhodotorula mucilaginosa. No marked difference was found in the principal coordinates analysis of the ordinations of yeast communities from the three sampling sites. The estimation using EstimateS software showed that the expected species richness was higher than the observed species richness. As the marine sponge–yeast association remains unclear, more systematic investigations should be carried out.
Similar content being viewed by others
References
Bell JJ, Barnes DKA (2000) A sponge diversity centre within a marine ‘island.’ Hydrobiologia 440:55–64
Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G (2010) Marine culturable yeasts in deep-sea hydrothermal vents: Species richness and association with fauna. FEMS Microbiol Ecol 73:121–133
Butinar L, Santos S, Spencer-Martins I, Oren A, Gunde-Cimerman N (2005) Yeast diversity in hypersaline habitats. FEMS Microbiol Lett 244:229–234
Calabon MS, Sadaba RB, Campos WL (2019) Fungal diversity of mangrove-associated sponges from New Washington, Aklan, Philippines. Mycology 10:6–21
Chen YS, Yanagida F, Chen LY (2009) Isolation of marine yeasts from coastal waters of northeastern Taiwan. Aquat Biol 8:55–60
Chi Z, Liu GL, Lu Y, Jiang H, Chi ZM (2016) Bio-products produced by marine yeasts and their potential applications. Bioresour Technol 202:244–252
Colwell R (2006) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. User’s Guide and Application. http://viceroy.eeb.uconn.edu/EstimateS. Accessed 27 March 2020
Demerdash AEl, Atanasov AG, Bishayee A, Abdel-Mogib M, Hooper JNA, Al-Mourabit A (2018) Batzella, Crambe and Monanchora: Highly prolific marine sponge genera yielding compounds with potential applications for cancer and other therapeutic areas. Nutrients 10:33. https://doi.org/10.3390/nu10010033
Duarte AWF, Dayo-Owoyemi I, Nobre FS, Pagnocca FC, Chaud LCS, Pessoa A, Felipe MGA, Sette LD (2013) Taxonomic assessment and enzymes production by yeasts isolated from marine and terrestrial Antarctic samples. Extremophiles 17:1023–1035
Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1371
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Gadanho M, Sampaio JP (2005) Occurrence and diversity of yeasts in the Mid-Atlantic Ridge hydrothermal fields near the Azores archipelago. Microb Ecol 50:408–417
Gadanho M, Almeida JMF, Sampaio JP (2003) Assessment of yeast diversity in a marine environment in the south of Portugal by microsatellite-primed PCR. A van Leeuwenhoek 84:217–227
Galstoff PS (1942) Wasting disease causing mortality of sponges in the West Indies and Gulf of Mexico. In: Proceedings of the eighth American science congress, vol 3, pp 411–412
Gao Z, Li B, Zheng C, Wang G (2008) Molecular detection of fungal communities in the Hawaiian marine sponges Suberites zeteki and Mycale armata. Appl Environ Microbiol 74:6091–6101
Godinho VM, de Paula MTR, Silva DAS, Paresque K, Martins AP, Colepicolo P, Rosa CA, Rosa LH (2019) Diversity and distribution of hidden cultivable fungi associated with marine animals of Antarctica. Fungal Biol 123:507–516
Gotelli NJ, Colwell RK (2011) Estimating Species Richness. Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54
Gümral R, Ozhak-Baysan B, Tümgor A, Saraclí MA, Yíldíran ST, Ilkit M, Zupančič J, Novak Babič M, Gunde-Cimerman N, Zalar P, de Hoog GS (2016) Dishwashers provide a selective extreme environment for human-opportunistic yeast-like fungi. Fungal Divers 76:1–9
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Hentschel U, Hopke J, Horn J, Friedrich A, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Envir Microbiol 68:4431
Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177
Huang CH, Lee FL, Tien CJ, Hsieh PW (2011) Rhodotorula taiwanensis sp. nov., a novel yeast species from a plant in Taiwan. A van Leeuwenhoek 99:297–302
Into P, Potes A, Sampaio JP, Limtong S (2020) Yeast diversity associated with the phylloplane of corn plants cultivated in Thailand. Microorganisms 8:80. https://doi.org/10.3390/microorganisms8010080
Jiang S, Sun W, Chen M, Dai S, Zhang L, Liu Y, Lee KJ, Li X (2007) Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp. A van Leeuwenhoek 92:405–416
Kaewkrajay C, Chanmethakul T, Limtong S (2020) Assessment of diversity of culturable marine yeasts associated with corals and zoanthids in the Gulf of Thailand. South China Sea. Microorganisms 8:474. https://doi.org/10.3390/microorganisms8040474
Khunnamwong P, Jindamorakot S, Limtong S (2018) Endophytic yeasts diversity in leaf tissue of rice, corn and sugarcane cultivated in Thailand assessed by a culture-dependent approach. Fungal Biol. https://doi.org/10.1016/j.funbio.2018.04.006
Kimura MA (1980) simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kiran GS, Sekar S, Ramasamy P, Thinesh T, Hassan S, Lipton AN, Ninawe AS, Selvin J (2018) Marine sponge microbial association: Towards disclosing unique symbiotic interactions. Mar Environ Res. https://doi.org/10.1016/j.marenvres.2018.04.017
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Kunthiphun S, Chokreansukchai P, Hondee P, Tanasupawat S, Savarajara A (2018) Diversity and characterization of cultivable oleaginous yeasts isolated from mangrove forests. World J Microbiol Biotechnol 34:125
Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. A van Leeuwenhoek 73:331–371
Kurtzman CP, Fell JW, Boekhout T (2011) The yeast a taxonomic study, 5th edn. Elsevier, Amsterdam
Kutty SN, Philip R (2008) Marine yeasts—a review. Yeast 25:465–483
Lages F, Silva-Graca M, Lucas A (1999) Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiology 145:2577–2585
Lahav R, Fareleira P, Nejidat A, Abeliovich A (2002) The identification and characterization of osmotolerant yeast isolates from chemical wastewater evaporation ponds. Microb Ecol 43:338–396
Laich F, Chávez R, Vaca I (2014) Leucosporidium escuderoi f.a., sp. nov., a basidiomycetous yeast associated with an Antarctic marine sponge. A van Leeuwenhoek 105:593–601
Li Z (2019) Sponge and coral microbiomes. In: Li Z (ed) Symbiotic microbiomes of coral reefs sponges and corals. Springer, Berlin, pp 17–28
Li Q, Wang G (2009) Diversity of fungal isolates from three Hawaiian marine sponges. Microbiol Res 164:233–241
Li Y, Ye D, Chen X, Lu X, Shao Z, Zhang H, Che Y (2009) Breviane spiroditerpenoids from an extreme-tolerant Penicillium sp. isolated from a deep sea sediment sample. J Nat Prod 75:912–916
Limtong S, Yongmanitchai W, Tun MM, Kawasaki H, Seki T (2007) Kazachstania siamensis sp. nov., an ascomycetous yeast species from forest soil in Thailand. Int J Syst Evol Microbiol 57:419–422
Limtong S, Kaewwichian R, Yongmanitchai W, Kawasaki H (2014) Diversity of culturable yeasts in phylloplane of sugarcane in Thailand and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 30:1785–1796
Liu WC, Li CQ, Zhu P, Yang JL, Cheng KD (2010) Phylogenetic diversity of culturable fungi associated with two marine sponges: Haliclona simulans and Gelliodes carnosa, collected from the Hainan Island coastal waters of the South China Sea. Fungal Divers 42:1–15
Loureiro STA, de Queiroz-Cavalcanti MA, Neves RP, de Oliveira-Passavante JZ (2005) Yeasts isolated from sand and sea water in beaches of Olinda, Pernambuco state, Brazil. Braz J Microbiol 36:1–8
Maldonado M, Cortadellas N, Trillas MI, Ruetzler K (2005) Endosymbiotic yeast maternally 851 transmitted in a marine sponge. Biol Bull 209:94–106
McIntyre FD, Drewery J, Eerkes-Medrano D, Neat FC (2016) Distribution and diversity of deep-sea sponge grounds on the Rosemary Bank Seamount NE Atlantic. Mar Biol 163:143. https://doi.org/10.1007/s00227-016-2913-z
Nagano Y, Nagahama T, Hatada Y, Nonoura T, Takami H, Miyazaki J, Takai K, Horikoshi K (2010) Fungal diversity in deep-sea sediments—the presence of novel fungal groups. Fungal Ecol 3:316–325
Naim MA, Smidt H, Sipkema D (2017) Fungi found in Mediterranean and North Sea sponges: How specific are they? PeerJ 5:e3722
Nakase T, Jindamorakot S, Am-In S, Ninomiya S, Kawasaki H, Limtong S (2009) Candida nonsorbophila sp. nov., a new ascomycetous yeast species isolated in Thailand. FEMS Yeast Res 9:663–667
Norkrans B (1966) Studies on marine occurring yeasts: growth related to pH, NaCl concentration and temperature. Arch Mikrobiol 54:374–392
Pagnocca FC, Mendonca-Hagler LC, Hagler AN (1989) Yeasts associated with the white shrimp Penaeus schmitti, sediment and water of Sepetiba Bay, Rio de Janeiro, Brazil. Yeast 5:5479–5483
Papadakis JS, Mavridou A, Richardson SC, Lamprini M, Marcelou U (1997) Bather-related microbial and yeast populations in sand and seawater. Water Res 31:799–804
Passarini MR, Miqueletto PB, de Oliveira VM, Sette LD (2014) Molecular diversity of fungal and bacterial communities in the marine sponge Dragmacidon reticulatum. J Basic Microbiol 55:207–220
Paulino GVB, Félix CR, Broetto L, Landell MF (2017) Diversity of culturable yeasts associated with zoanthids from Brazilian reef and its relation with anthropogenic disturbance. Mar Pollut Bull 123:253–260
Phaff HJ, Mrak EM, Williams OB (1952) Yeasts isolated from shrimp. Mycologia 44:431–451
Pile AJ, Patterson MR, Witman JD (1996) In situ grazing on plankton < 10 um by the boreal sponge Mycale lingua. Mar Ecol Prog Ser 141:95–102
Poli A, Vizzini A, Prigione V, Varese GC (2018) Basidiomycota isolated from the Mediterranean Sea-Phylogeny and putative ecological roles. Fungal Ecol 36:51–62
Prabhakaran N, Gupta R (1991) Yeasts from the sediment samples of the EEZ along the southwest coast of India. J Mar Biol Assoc India 33:455
Putchakarn S (2007) Species diversity of marine sponges dwelling in coral reefs in Had Khanom—Mo Ko Thale Tai National Park, Nakhon Si Thammarat Province, Thailand. J Mar Biolog Assoc UK 87:1635–1642
Rédou V, Navarri M, Meslet-Cladieŕe L, Barbier G, Burgaud G (2015) Species richness and adaptation of marine fungi from deep-subseafloor sediments. Appl Environ Microbiol 81:3571–3583
Reiswig HM (1974) Water transport respiration and energetics of 3 tropical marine sponges. J Exp Mar Biol Ecol 14:231–249
Ruiz-Barba JL, Maldonado A, Jiménez-Díaz R (2005) Small-scale total DNA extraction from bacteria and yeast for PCR applications. Anal Biochem 347:333–335
Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (2000) Introduction to food- and airborne fungi. Centraalbureau voor Schimmelcultures, Utrecht, p 389
Satianpakiranakorn P, Khunnamwong P, Limtong S (2020) Yeast communities of secondary peat swamp forests in Thailand and their antagonistic activities against fungal pathogens cause of plant and postharvest fruit diseases. PLoS ONE 15(3):e0230269. https://doi.org/10.1371/journal.pone.0230269
Selvin J, Ninawe AS, Kiran GS, Lipton AP (2010) Sponge-microbial interactions: ecological implications and bioprospecting avenues. Crit Rev Microbiol 36:82–90
Seshadri R, Sieburth J (1971) Cultural estimation of yeasts on seaweeds. Appl Microbiol 22:507–512
Simister RL, Deines P, Botté ES, Nicole S, Webster NS, Taylor MW (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14:517–524
Singh P, Raghukumar C, Meena RM, Verma P, Shouche Y (2012) Fungal diversity in deep sea sediments revealed by culture-dependent and culture-independent approaches. Fungal Ecol 5:543–553
Sparks AK (1985) Synopsis of invertebrate pathology: exclusive of insects. Elsevier, New York
Srisuk N, Nutaratat P, Surussawadee J, Limtong S (2019) Yeast communities in sugarcane phylloplane. Microbiology 88:353–369
Sugita T, Nakase T (1998) Trichosporon japonicum sp. nov. isolated from the air. Int J Syst Bacteriol 48:1425–1429
Sugiyama Y, Ito Y, Suzuki M, Hirota A (2009) Indole derivatives from a marine sponge-derived yeast as DPPH radical scavengers. J Nat Prod 72:2069–2071
Sweih NAl, Ahmad S, Khan S, Khan Z, Joseph L, Vayalil S, Chandy R (2017) Persistent Candida conglobata bloodstream infection in a preterm neonate successfully treated by combination therapy with amphotericin B and caspofungin. J Mycol Med 27:271–276
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Molec Biol Rev 71:295–347
Thakur NL, Muller WEG (2004) Biotechnological potential of marine sponges. Curr Sci 86:1506–1512
Trautman DA, Hinde R (2001) Sponge/algal symbioses: a diversity of associations, In: Seckbach J (ed) Cellular origin, life in extreme habitats and astrobiology, vol. 4. Springer, Dordrecht, pp 521–537
Vaca I, Faúndez C, Maza F, Paillavil B, Hernández V, Acosta F, Levicán G, Martínez C, Chávez R (2013) Cultivable psychrotolerant yeasts associated with Antarctic marine sponges. World J Microbiol Biotechnol 29:183–189
Vacelet J (1975) Electron microscope study of the association between bacteria and sponges of the genus Verongia Dictyoceratida. J Exp Mar Biol Ecol 23:271–288
Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314
Vacelet J, Vacelet E, Gaino E, Gallissian MF (1994) Bacterial attach of sponging skeleton during the 1986–1990 Mediterranean sponge disease. In: van Soest RWM, van Kempen TMG, Braekman JC (eds) Sponges in time and space. Rotterdam, AA Balkema p, pp 355–362
van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez B, Hajdu E, Pisera AB, Manconi R, Schönberg C, Klautau M, Kelly M, Vacelet J, Dohrmann M, Díaz MC, Cárdenas P, Carballo JL, Ríos P, Downey R, Morrow CC (2020) World Porifera Database. http://www.marinespecies.org/porifera. Accessed 31 March 2020
van Uden N, Fell JW (1968) Marine yeasts Adv Microbiol Sea 1:167–201
Viyakarn V, Chavanich S, Heery E, Raksasab C (2020) Distribution of sea cucumbers, Holothuria atra, on reefs in the upper Gulf of Thailand and the effect of their population dinsities on sediment microalgal productivity. Estuar Coast Shelf Sci 235:106514
Vogel S (1977) Current-induced flow through living sponges in nature. Proc Natl Acad Sci USA 74:2069–2071
Vogel C, Rogerson A, Schatz S, Laubach H, Tallman A, Fell J (2007) Prevalence of yeasts in beach sand at three bathing beaches in South Florida. Water Res 41:1915–1920
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322
Wilborn R, Rooper CN, Goddard P, Li L, Williams K, Towler R (2018) The potential effects of substrate type, currents, depth and fishing pressure on distribution, abundance, diversity, and height of cold-water corals and sponges in temperate, marine waters. Hydrobiologia 811:251–268
Xu W, Pang KL, Luo ZH (2014) High fungal diversity and abundance recovered in the deep-sea sediments of the Pacific Ocean. Microb Ecol 68:688–698
Yang SP, Wu ZH, Jian JC (2011) Distribution of marine red yeasts in shrimps and the environments of shrimp culture. Curr Microbiol 62:1638–1642
Zalar P, Novak M, de Hoog GS, Gunde-Cimerman N (2011) Dishwashers—a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol 115:997–1007
Zhang X, Hua M, Song C, Chi Z (2012) Occurrence and diversity of marine yeasts in Antarctica environments. J Ocean Univ China 11:70–74
Zhang XY, Tang GL, Xu XY, Nong XH, Qi SH (2014) Insights into deep-sea sediment fungal communities from the East Indian Ocean using targeted environmental sequencing combined with traditional cultivation. PLoS ONE 9:e109118
Zu P, Li Q, Wang G (2008) Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. Microb Ecol 55:406–414
Acknowledgements
The authors would like to thank the Plant Genetic Conservation Project under the Royal Initiative of Her Royal Highness Princess Maha Chakri Sirindhorn for supporting marine organism collection.
Funding
This research was funded by the Thailand Research Fund (TRF) through a TRF Team Promotion Grant (RTA 6080004).
Author information
Authors and Affiliations
Contributions
C.K.: Performed research and wrote the paper, S.P.: Performed research, S.L.: Designed study, data discussion and wrote the paper.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that there are no conflicts of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors. The Thailand Animal Science Act 2015 defines animals as not including marine sponges.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Rights and permissions
About this article
Cite this article
Kaewkrajay, C., Putchakarn, S. & Limtong, S. Cultivable yeasts associated with marine sponges in the Gulf of Thailand, South China Sea. Antonie van Leeuwenhoek 114, 253–274 (2021). https://doi.org/10.1007/s10482-021-01518-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-021-01518-6