Abstract
We isolated and characterized the community of cultivable fungi associated with marine macroalgae present in the Magellan sub-Antarctic straits and the South Shetland Islands, Maritime Antarctica, and evaluated their production of bioactive metabolites. A total of 201 filamentous fungal isolates were obtained. The genera Antarctomyces, Pseudogymnoascus, Microdochium, Trichoderma, Cladosporium, Penicillium, Neoascochyta, Entomortierella and Linnemannia were associated with Antarctic macroalgae, with Neoascochyta paspali being the most abundant taxon. In contrast, 12 taxa representing Cadophora, Microdochium, Penicillium, Pseudogymnoascus were associated with macroalgae from the Magellan sub-Antarctic, with Penicillium dominating the assemblages. The diversity indices of the fungal communities associated with macroalgae in the two regions were similar. Among 177 fungal extracts assessed for metabolite production, 31 (17.5%) showed strong phytotoxic activity and 17 (9.6%) showed anti-Trypanosoma cruzi activity. Penicillium showed the highest phytotoxic and anti-Trypanosoma activity values. The detection of taxa in common between the polar and cold temperate zones reinforces the need for further investigations of the distribution of species in these distinct ecoregions. The detection of bioactive extracts produced particularly by Penicillium representatives reinforces the potential to obtain active molecules that can be explored as natural products or as sources of bioactive compounds with application in agriculture and biomedicine.





Similar content being viewed by others
Data availability
All fungal sequences were deposited in the NCBI database.
References
Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014) Jvenn: an interactive Venn diagram viewer. BMC Bioinform 15:293. https://doi.org/10.1186/1471-2105-15-293
Bugni TS, Ireland CM (2004) Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 21:143–163
Callahan HL, Portal AC, Devereaux R, Grogl M (1997) An axenic amastigote system for drug screening. Antimicrob Agents Chemother 41:818–822. https://doi.org/10.1128/AAC.41.4.818
Camus PA (2001) Marine biogeography of continental Chile. Rev Chil Hist Nat 74:587–617
Castellani A (1967) Maintenance and cultivation of common pathogenic fungi in distilled water. J Trop Med Hygien 42:181–184
Coelho LC, de Carvalho CR, Rosa CA et al (2021) Diversity, distribution, and xerophilic tolerance of cultivable fungi associated with the Antarctic angiosperms. Polar Biol 44:379–388. https://doi.org/10.1007/s00300-021-02799-3
da Silva MK, Barreto DLC, Vieira R et al (2024) Diversity and enzymatic, biosurfactant and phytotoxic activities of culturable Ascomycota fungi present in marine sediments obtained near the South Shetland Islands, maritime Antarctica. Extremophiles 28:20. https://doi.org/10.1007/s00792-024-01336-4
de Menezes GCA, Godinho VM, Porto BA, Gonçalves VN, Rosa LH (2017) Antarctomyces pellizariae sp. nov., a new, endemic, blue, snow resident psychrophilic ascomycete fungus from Antarctica. Extremophiles 21:259–269. https://doi.org/10.1007/s00792-016-0895-x
Duarte AWF, Passarini MRZ, Delforno TP, Pelizzari FM, Cipro CVZ, Montene RC, Petry MV, Putzke J, Rosa LH, Sette LD (2016) Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Environm Microbiol 8:874–885. https://doi.org/10.1111/1758-2229.12452
Furbino LE, Godinho VM, Santiago IF, Pellizari FM et al (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microb Ecol 67:775–787. https://doi.org/10.1007/s00248-014-0374-9
Furbino LE, Pellizzari FM, Neto PC, Rosa CA, Rosa LH (2017) Isolation of fungi associated with macroalgae from maritime Antarctica and their production of agarolytic and carrageenolytic activities. Polar Biol 41:527–535. https://doi.org/10.1007/s00300-017-2213-1
Godinho VM, Furbino LE, Santiago IF et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451. https://doi.org/10.1038/ismej.2013.77
Godinho VM, Gonçalves VN, Santiago IF et al (2015) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585–596. https://doi.org/10.1007/s00792-015-0741-6
Gomes ECQ, Godinho VM, Silva DAS et al (2018) Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22:381–393. https://doi.org/10.1007/s00792-018-1003-1
Gómez I, Huovinen P (2020) Antarctic seaweeds: biogeography, adaptation, and ecosystem services. In: Gómez I, Huovinen P (eds) Antarctic seaweeds. Springer, Cham. https://doi.org/10.1007/978-3-030-39448-6_1
Gonçalves VN, Vaz ABM, Rosa CA, Rosa LH (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82:459–471. https://doi.org/10.1111/j.1574-6941.2012.01424.x
Gonçalves MFM, Esteves AC, Alves A (2020) Revealing the hidden diversity of marine fungi in Portugal with the description of two novel species, Neoascochyta fuci sp. nov. and Paraconiothyrium salinum sp. nov. Int J Syst Evol 70:5337–5354. https://doi.org/10.1099/ijsem.0.004410
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Lieckfeldt E, Meyer W, Börner T (1993) Rapid identification and differentiation of yeasts by DNA and PCR fingerprinting. J Basic Microbiol 33:413–426. https://doi.org/10.1002/jobm.3620330609
Loque CP, Medeiros AO, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648. https://doi.org/10.1007/s00300-009-0740-0
Mansilla A, Rosenfeld S, Rendoll J et al (2014a) Tolerance response of Lessonia flavicans from the sub-Antarctic ecoregion of Magallanes under controlled environmental conditions. J Appl Phycol 26:1971–1977. https://doi.org/10.1007/s10811-014-0294-6
Mansilla A, Rosenfeld S, Rendoll J, Murcia S, Werlinger C, Yokoya NS, Terrados J (2014b) Tolerance response of Lessonia flavicans from the Sub-Antarctic ecoregion of Magallanes under controlled environmental conditions. J Appl Phycol 26:1971–1977
Martorell MM, Lannert M, Matula CV et al (2021) Studies toward the comprehension of fungal-macroalgae interaction in cold marine regions from a biotechnological perspective. Fungal Biol 125:218–230. https://doi.org/10.1016/j.funbio.2020.11.003
Ogaki MB, de Paula MT, Ruas D et al (2019) Marine fungi associated with Antarctic macroalgae. In: Castro-Sowinski S (ed) The ecological role of micro-organisms in the Antarctic environment. Springer Polar Sciences, Springer, Cham, pp 239–255. https://doi.org/10.1007/978-3-030-02786-5_11
Ogaki MB, Teixeira DR, Vieira R, Lírio JM, Felizardo JPS, Abuchacra RC, Cardoso RP, Zani CL, Alves TMA, Junior PAS, Murta SMF, Barbosa EC, Oliveira JG, Ceravolo IP, Pereira PO, Rosa CA, Rosa LH (2020a) Diversity and bioprospecting of cultivable fungal assemblages in sediments of lakes in the Antarctic Peninsula. Fungal Biol 124:601–611. https://doi.org/10.1016/j.funbio.2020.02.015. (Epub 2020 Mar 6)
Ogaki MB, Vieira R, Muniz MC, Zani CL, Alves TMA, Junior PAS, Murta SMF, Barbosa EC, Oliveira JG, Ceravolo IP, Pereira PO, Rosa CA, Rosa LH (2020b) Diversity, ecology, and bioprospecting of culturable fungi in lakes impacted by anthropogenic activities in Maritime Antarctica. Extremophiles 24:637–655. https://doi.org/10.1007/s00792-020-01183-z. (Epub 2020 Jun 13)
Ojeda J, Rosenfeld S, Marambio J, Rozzi R, Mansilla A (2014) Patrones estacionales y espaciales de la diversidad de moluscos intermareales de bahía Róbalo, canal Beagle, Reserva de la Biosfera Cabo de Hornos, Chile. Rev Biol Mar Oceanogr 49:493–509
Oliveira MC, Pellizzari F, Medeiros AS, Yokoya NS (2020) Diversity of Antarctic seaweeds. In: Gómez I, Huovinen P (eds) Antarctic seaweeds. Springer, Berlin, pp 23–42. https://doi.org/10.1007/978-3-030-39448-6_2
Pellizzari F, Silva MC, Medeiros A et al (2017) Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol 40:1671–1685. https://doi.org/10.1007/s00300-017-2092-5
Pellizzari F, Rosa LH, Yokoya NS (2020) Biogeography of Antarctic seaweeds facing climate changes. In: Gómez I (ed) Antarctic seaweeds. Springer International Publishing, Berlin, pp 83–102. https://doi.org/10.1007/978-3-030-39448-6_5
Raghukumar S (2017) Fungi in coastal and oceanic marine ecosystems. Springer, New York. https://doi.org/10.1007/978-3-319-54304-8
Romanha AJ, de Castro SL, Soeiro MNC et al (2010) In vitro and in vivo experimental models for drug screening and development for Chagas disease. Mem Inst Oswaldo Cruz 105:233–238. https://doi.org/10.1590/S0074-02762010000200022
Rosa LH, Vaz ABM, Caligiorne RB, Campolina S, Rosa CA (2009) Endophytic fungi associated with the Antarctic Grass Deschampsia antarctica Desv. (Poaceae). Polar Biol 32:161–167. https://doi.org/10.1007/s00300-008-0515-z
Rosa LH, Queiroz SCN, Moraes RM et al (2013) Coniochaeta ligniaria: antifungal activity of the cryptic endophytic fungus associated with autotrophic tissue cultures of the medicinal plant Smallanthus sonchifolius (Asteraceae). Symbiosis 60:133–142. https://doi.org/10.1007/s13199-013-0249-8
Rosa LH, Pellizzari FM, Ogaki MB et al (2019) Sub Antarctic and Antarctic marine ecosystems: an unexplored ecosystem of fungal diversity. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications. Springer, Berlin, pp 221–242. https://doi.org/10.1007/978-3-030-18367-7_10
Sanches PF, Pellizzari F, Horta PA (2016) Multivariate analyses of Antarctic and Sub-Antarctic seaweed distribution patterns: an evaluation of the role of the Antarctic Circumpolar Current. J Sea Res 110:29–38. https://doi.org/10.1016/j.seares.2016.02.002
Santiago IF, Alves TM, Rabello A, Junior PAS, Romanha AJ, Zani CL, Rosa CA, Rosa LH (2012) Leishmanicidal and antitumoral activities of endophytic fungi associated with the Antarctic angiosperms Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth) Bartl. Extremophiles 16:95–103
Santiago IF, Rosa CA, Rosa LH (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097. https://doi.org/10.1007/s00792-015-0781-y
Silva N, Calvete C (2002) Características oceanográficas físicas y químicas de canales australes chilenos entre el golfo de Penas y el Estrecho de Magallanes (Crucero CIMAR-FIORDOS 2). Cienc Tecnol Mar 25:23–88
Soto E, Báez P, Ramírez EM, Letelier S, Naretto J, Rebolledo A (2012) Biotopos marinos intermareales entre Canal Trinidad y Canal Smyth, Sur de Chile. Rev Biol Mar Oceanogr 47:177–191
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern S, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583
Stchigel AM, Cano J, MacCormack CW (2001) Antarctomyces psychrotrophicus gen. et sp. nov., a new ascomycete from Antarctica. Mycol Res 105:377–382. https://doi.org/10.1017/S0953756201003379
Suryanarayanan TS (2012a) Fungal endosymbionts of seaweeds. In: Raghukumar C (ed) Biology of marine fungi. Springer, Berlin, pp 53–70. https://doi.org/10.1007/978-3-642-23342-5_3
Suryanarayanan TS (2012b) Fungal endosymbionts of seaweeds. Biology of marine fungi. Springer, Berlin, pp 53–69
Suryanarayanan TS, Venkatachalam A, Thirunavukkarasu N, Ravishankar JP, Doble M, Geetha V (2010) Internal mycobiota of marine macroalgae from the Tamilnadu coast: distribution, diversity and biotechnological potential. Bot Mar 53:457–468
White TJ, Bruns TD, Lee SB (1990) Amplifcation and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis NA, Gelfand J, Sninsky J, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Acknowledgements
This study received financial support from CNPq, PROANTAR, CAPES and FAPEMIG. We thank Network of Technological Platforms from FIOCRUZ, for the support and financing of the services provided by the Platform Bioprospecção de Produtos Naturais-MG (RPT10A)/FIOCRUZ-Minas and Platform Bioensaios para triagem de drogas anti-Trypanosoma cruzi (PlaBio Tc). PC is supported by NERC core funding to the British Antarctic Survey’s ‘Biodiversity, Evolution and Adaptation’ Team. LHR, CLZ, TMAA and SMFM are CNPq research fellows.
Author information
Authors and Affiliations
Contributions
MSF, CRC, FMP, AOM, LHR conceived the study. AOM, JM, LHR performed the algal sampling. MSF, CRC performed the phytotoxic assays. TMAA, SMFM, CLZ performed the biological assays. MSF, CRC, FMP, AOM, JM, TMAA, SMFM, CLZ, PC, LHR analyzed the results and wrote the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by Oren.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Freitas, M.S., de Carvalho, C.R., Pellizzari, F.M. et al. Diversity, distribution and phytotoxic and anti-Trypanosoma activities of cultivable fungi associated with Magellan sub-Antarctic strait and Maritime Antarctic macroalgae. Extremophiles 28, 46 (2024). https://doi.org/10.1007/s00792-024-01363-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00792-024-01363-1

