Skip to main content

Advertisement

SpringerLink
Log in

Antifungal activity of carrageenan extracts from the red alga Chondracanthus teedei var. lusitanicus

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Carrageenans extracted from Chondracanthus teedei var. lusitanicus were studied in order to determine their potential antifungal activity. FTIR-ATR and FT-Raman spectroscopic analysis confirmed the presence of a hybrid kappa/iota carrageenan belonging to the gametophyte phase and a hybrid xi/theta carrageenan in the tetrasporophyte phase. Kappa/iota and xi/theta carrageenan induced the formation of swollen hyphal segments in Alternaria infectoria, upon exposure to 125 and 60 μg mL−1, respectively. The observed phenotype was similar to those induced by antifungals targeting the fungal cell wall. When exposed to 87.5 μg mL−1 of kappa/iota carrageenan, Aspergillus fumigatus hyphae became shortened and highly branched, a phenotype commonly observed in response to antifungals. These morphological alterations were associated with a decrease of the β-glucan content in A. infectoria after exposure to 150 μg mL−1 of kappa/iota and to 100 μg mL−1 of xi/theta carrageenan. On the other hand, the chitin cell wall content of A. fumigatus decreased significantly upon exposure to 150 μg mL−1 of both extracts, which triggered an increase in the content of β-glucan. Overall, the present work shows that carrageenans extracted from C. teedei var. lusitanicus cause alterations on the A. fumigatus and A. infectoria cell walls, indicating a marked antifungal activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anjos J, Fernandes C, Silva BM, Quintas C, Abrunheiro A, Gow NAR, Gonçalves T (2012) β(1,3)-Glucan synthase complex from Alternaria infectoria, a rare dematiaceous human pathogen. Med Mycol 50:716–725

  • Baddley JW, Pappas PG, Smith AC, Moser SA (2003) Epidemiology of Aspergillus terreus at a university hospital. J Clin Microbiol 41:5525–5529

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhakuni DS, Rawat DS (2005) Bioactive marine natural products. Springer, Netherlands

    Google Scholar 

  • Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335

    Article  Google Scholar 

  • Bowman JC, Hicks PS, Kurtz MB, Rosen H, Schmatz DM, Liberator PA, Douglas CM (2002) The antifungal echinocandin caspofungin acetate kills growing cells of Aspergillus fumigatus in vitro. Antimicrob Agents Chemother 46:3001–3012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braga MRA (1985) Taxonomia e biologia da Gigartina teedii (Roth) Lamouroux (Rhodophyta, Gigartinales) no litoral do estado de São Paulo. Dissertation, Univ. São Paulo

  • Braga MRA (1990) Reproductive characteristics of Gigartina teedii (Roth) Lamouroux (Rhodophyta, Gigartinales), a turf-forming species - Field and laboratory culture studies. Bot Mar 33:401–409

    Google Scholar 

  • Campo VL, Kawano DF, da Silva DB, Carvalho I (2009) Carrageenans: biological properties, chemical modifications and structural analysis—a review. Carbohydr Polym 77:167–180

    Article  CAS  Google Scholar 

  • Cardoso SM, Carvalho LG, Silva PJ, Rodrigues MS, Pereira OR, Pereira L (2014) Bioproducts from macroalgae: a review with focus on the Iberian Peninsula. Curr Org Chem 18:896–917

    Article  CAS  Google Scholar 

  • Chopin T, Kerin BF, Mazerolle R (1999) Phycocolloid chemistry as a taxonomic indicator of phylogeny in the Gigartinales, Rhodophyceae: a review and current developments using Fourier transform infrared diffuse reflectance spectroscopy. Phycol Res 47:167–188

    Article  CAS  Google Scholar 

  • Fernandes C, Anjos J, Walker LA, Silva BM, Cortes L, Mota M, Munro CA, Gow NA, Gonçalves T (2014) Modulation of Alternaria infectoria cell wall chitin and glucan synthesis by cell wall synthase inhibitors. Antimicrob Agents Chemother 58:2894–2904

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandes C, Prados-Rosales R, Silva B, Nakouzi-Naranjo A, Zuzarte M, Chatterjee S, Stark RE, Casadevall A, Gonçalves T (2016) Activation of melanin synthesis in Alternaria infectoria by antifungal drugs. Antimicrob Agents Chemother 60:1646–55

    Article  PubMed Central  Google Scholar 

  • Flemming RV, Walsh TJ, Anaissie EJ (2002) Emerging and less common fungal pathogens. Infect Dis Clin 16:915–933

    Article  Google Scholar 

  • Gayral P (1982) Les algues de côtes Françaises (Manche & Atlantique). Éditions Doin: 21–29

  • Guiry MD (1984) Structure, life-history and hybridization of Atlantic Gigartina teedii (Rhodophyta) in culture. Brit Phycol J 19:37–55

    Article  Google Scholar 

  • Hajjeh RA, Sofair AN, Harrison LH, Lyon GM, Arthington-Skaggs BA, Mirza SA, Phelan M, Morgan J, Lee-Yang MA, Ciblak LE et al (2004) Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol 42:1519–1527

    Article  PubMed  PubMed Central  Google Scholar 

  • Hector RF (1993) Compounds active against cell walls of medically important fungi. Clin Microbiol Rev 6:1–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hohl TM, Feldmesser M (2007) Aspergillus fumigatus: principles of pathogenesis and host defense. Eukaryot Cell 6:1953–1963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    Article  CAS  Google Scholar 

  • Iwen PC, Rupp ME, Langnas AN, Reed EC, Hinrichs SH (1998) Invasive pulmonary aspergillosis due to Aspergillus terreus: 12-year experience and review of the literature. Clin Infect Dis 26:1092–1097

    Article  CAS  PubMed  Google Scholar 

  • Jiao G, Yu G, Zhang J, Ewart HS (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalitnik AA, Byankina Barabanova AO, Nagorskaya VP, Reunov AV, Glazunov VP, Solov’eva TF, Yermak IM (2012) Low molecular weight derivatives of different carrageenan types and their antiviral activity. J Appl Phycol 25:65–72

    Article  Google Scholar 

  • Kalitnik AA, Anastyuk SD, Sokolova EV, Kravchenko AO, Khasina EI, Yermak IM (2015) Oligosaccharides of κ/β-carrageenan from the red alga Tichocarpus crinitus and their ability to induce interleukin 10. J Appl Phycol 28:545–553

    Article  Google Scholar 

  • König G, Wright A, Sticher O, Angerhofer C, Pezzuto J (1994) Biological activities of selected marine natural products. Planta Med 60:532–537

    Article  PubMed  Google Scholar 

  • Lopes G, Pinto E, Andrade PB, Valentão P (2013) Antifungal activity of phlorotannins against dermatophytes and yeasts: approaches to the mechanism of action and influence on Candida albicans virulence factor. PLoS One 8:e72203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer AMS, Rodríguez AD, Berlinck RGS, Hamann MT (2007) Marine pharmacology in 2003–4: marine compounds with anthelmintic antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems, and other miscellaneous mechanisms of action. Comp Biochem Physiol C 145:553–581

    Google Scholar 

  • McCandless EL, West JA, Guiry MD (1982) Carrageenan patterns in the Phyllophoraceae. Biochem Syst Biol 10:275–84

    CAS  Google Scholar 

  • McCandless EL, West JA, Guiry MD (1983) Carrageenan patterns in the Gigartinaceae. Biochem Syst Biol 11:175–82

    Article  CAS  Google Scholar 

  • Mirza SA, Phelan M, Rimland D, Graviss E, Hamill R, Brandt ME, Gardner T, Sattah M, Ponce de Leon G, Baughman W, Hajjeh RA (2003) The changing epidemiology of cryptococcosis: an update from population-based active surveillance in 2 large metropolitan areas, 1992–2000. Clin Infect Dis 36:789–794

    Article  PubMed  Google Scholar 

  • Munro CA, Winter K, Buchan A, Henry K, Becker JM, Brown AJ, Bulawa CE, Gow NA (2001) Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and for cell integrity. Mol Microbiol 39:1414–1426

  • Murray PM, Moane S, Collins C, Beletskaya T, Thomas OP, Duarte AWF, Nobre FS, Owoyemi IO, Pagnocca FC, Sette LD, McHugh E, Causse E, Pérez-López P, Feijoo G, Moreira MT, Rubiolo J, Leirós M, Botana LM, Pinteus S, Alves C, Horta A, Pedrosa R, Jeffryes C, Agathos SN, Allewaert C, Verween A, Vyverman W, Laptev I, Sineoky S, Bisio A, Manconi R, Ledda F, Marchi M, Pronzato R, Walsh DJ (2013) Sustainable production of biologically active molecules of marine based origin. Nat Biotechnol 30:839–850

    CAS  Google Scholar 

  • Muszkieta L, Aimanianda V, Mellado E, Gribaldo S, Alcàzar-Fuoli L, Szewczyk E, Prevost MC, Latgé JP (2014) Deciphering the role of the chitin synthase families 1 and 2 in the in vivo and in vitro growth of Aspergillus fumigatus by multiple gene targeting deletion. Cell Microbiol 16:1784–1805

    Article  CAS  PubMed  Google Scholar 

  • Pangestuti R, Kim SK (2014) Biological activities of carrageenan. Adv Food Nutr Res 72:113–124

    Article  CAS  PubMed  Google Scholar 

  • Patel S (2012) Therapeutic importance of sulfated polysaccharides from seaweeds: updating the recent findings. Biotech 3(2):171–185

    Google Scholar 

  • Perea S, Thomas F (2002) Patterson antifungal resistance in pathogenic fungi. Clin Infect Dis 35:1073–1080

    Article  PubMed  Google Scholar 

  • Pereira L (2004) Estudos em macroalgas carragenófitas (Gigartinales, Rhodophyceae) da costa portuguesa—aspectos ecológicos, bioquímicos e citológicos. Dissertation, University of Coimbra

  • Pereira L (2006) Identification of phycocolloids by vibrational spectroscopy. In: Critchley AT, Ohno M, Largo DB (Eds) World seaweed resources—an authoritative reference system. ETI Information Services Ltd

  • Pereira L (2012) Cytological and cytochemical aspects in selected carrageenophytes (Gigartinales, Rhodophyta). In: K. Heimann and C. Katsaros (eds) Advances in Algal Cell Biology. De Gruyter, Berlin, pp 81–104

  • Pereira L, Mesquita JF (2004) Population studies and carrageenan properties of Chondracanthus teedei var. lusitanicus (Gigartinaceae, Rhodophyta). J Appl Phycol 16:369–383

    Article  CAS  Google Scholar 

  • Pereira L, van de Velde F (2011) Portuguese carrageenophytes: carrageenan composition and geographic distribution of eight species (Gigartinales, Rhodophyta). Carbohydr Polym 84:614–623

    Article  CAS  Google Scholar 

  • Pereira L, Sousa A, Coelho H, Amado AM, Ribeiro-Claro PJA (2003) Use of FTIR, FT-Raman and 13C-NMR spectroscopy for identification of some seaweed phycocolloids. Biomol Eng 20:223–228

    Article  CAS  PubMed  Google Scholar 

  • Pereira L, van de Velde F, Mesquita JF (2007) Cytochemical studies on underutilized carrageenophytes (Gigartinales, Rhodophyta). BIBIEN 1:1–5

    Google Scholar 

  • Pereira L, Amado AM, Critchley AT, van de Velde F, Ribeiro-Claro PJA (2009) Identification of selected seaweed polysaccharides (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). Food Hydrocoll 23:1903–1909

    Article  CAS  Google Scholar 

  • Perez R, Kaas R, Campello F, Arbault S, Baarbaroux O (1992) La Culture des algues marines dans le monde. IFREMER, Plouzane

    Google Scholar 

  • Pfaller MA, Diekema DJ (2004) Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J Clin Microbiol 42:4419–4431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinteus S, Alves C, Monteiro H, Araujo E, Horta A, Pedrosa R (2015) Asparagopsis armata and Sphaerococcus coronopifolius as a natural source of antimicrobial compounds. World J Microbiol Biotechnol 31:445–451

    Article  PubMed  Google Scholar 

  • Prajapati VD, Pankaj MM, Girish KJ, Himanshu KS (2014) Carrageenan: a natural seaweed polysaccharide and its applications. Carbohydr Polym 105:97–112

    Article  CAS  PubMed  Google Scholar 

  • Richardson MD, Warnock DW (2012) Fungal infection: diagnosis and management. Wiley-Blackwell, Oxford

    Book  Google Scholar 

  • Rudolph B (2000) Seaweed products: red algae of economic significance. In: Martin RE (ed) Marine & freshwater products handbook. Technomic Pub Co, Lancaster, pp 515–529

    Google Scholar 

  • Salvador N, Gómez Garreta A, Lavelli L, Ribera MA (2007) Antimicrobial activity of Iberian macroalgae. Sci Mar 71:101–114

    Article  Google Scholar 

  • Singh N (2001) Trends in the epidemiology of opportunistic fungal infections: predisposing factors and the impact of antimicrobial use practices. Clin Infect Dis 33:1692–1696

    Article  CAS  PubMed  Google Scholar 

  • Stanley NF (1987) Production, properties and use of carrageenans. In: McHugh DJ (ed) Production and utilization of products from commercial seaweeds. FAO, Rome, pp 97–147

    Google Scholar 

  • Verwer PEB, van Duijn ML, Tavakol M, Bakker-Woudenberg IAJM, van de Sande WWJ (2012) Reshuffling of Aspergillus fumigatus cell wall components chitin and β-glucan under the influence of caspofungin or nikkomycin Z alone or in combination. Antimicrob Agents Chemother 56:1595–1598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh TJ, Groll A, Hiemenz J, Flemming R, Roilides E, Anaissie E (2004) Infections due to emerging and uncommon medically important fungal pathogens. Clin Microbiol Infect 10:48–66

    Article  PubMed  Google Scholar 

  • Yermak IM, Khotimchenko YS (2003) In: Fingerman M, Nagabhushanam R (eds). Recent advances in marine biotechnology. Science Publishers: Enfield. pp 207–255

  • Yuan H, Song J, Li X, Li N, Liu S (2010) Enhanced immunostimulatory and antitumor activity of different derivatives of κ-carrageenan oligosaccharides from Kappaphycus striatum. J Appl Phycol 23:59–65

    Article  Google Scholar 

  • Zinoun M, Cosson J (1996) Seasonal variation in growth and carrageenan content of Calliblepharis jubata (Rhodophyceae, Gigartinales) from the Normandy coast, France. J Appl Phycol 8:29–34

    Article  Google Scholar 

Download references

Acknowledgments

We thank Prof. P. Ribeiro-Claro, Department of Chemistry, CICECO, University of Aveiro, for FTIR and FT-Raman spectroscopy.

This study was partly supported by FEDER funds through the Operational Programme Competitiveness Factors-COMPETE and national funds by FCT-Foundation for Science and Technology under the strategic project UID/NEU/04539/2013. C. Fernandes is a recipient of a postdoctoral fellowship from FCT-Fundação para a Ciência e Tecnologia (SFRH/BPD/63733/2009). The authors also acknowledge financial support from the Portuguese Foundation for Science and Technology through Institute of Marine Research (IMAR) and Marine and Environmental Sciences Centre (MARE).

Authors’ contributions

F. Soares performed the experimental work and wrote part of the manuscript; C. Fernandes collaborated, designed, and supervised the lab work and revised the manuscript; P. Silva collaborated and set up most of the lab techniques; L. Pereira designed part of the study and revised the data and the manuscript; T. Gonçalves designed part of the study, antifungal data interpretation, and manuscript revision.

Author information

Authors and Affiliations

  1. MARE – Marine and Environmental Sciences Centre/IMAR – Institute of Marine Research, Department of Life Sciences, University of Coimbra, 3000-456, Coimbra, Portugal

    Fabiana Soares, Paulo Silva & Leonel Pereira

  2. CNC – Center for Neurosciences and Cell Biology, University of Coimbra, Rua Larga, 3004-504, Coimbra, Portugal

    Chantal Fernandes & Teresa Gonçalves

  3. FMUC – Faculty of Medicine, University of Coimbra, Rua Larga, 3004-504, Coimbra, Portugal

    Teresa Gonçalves

Authors
  1. Fabiana Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chantal Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paulo Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonel Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Teresa Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chantal Fernandes.

Additional information

L. Pereira and T. Gonçalves share senior authorship.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soares, F., Fernandes, C., Silva, P. et al. Antifungal activity of carrageenan extracts from the red alga Chondracanthus teedei var. lusitanicus . J Appl Phycol 28, 2991–2998 (2016). https://doi.org/10.1007/s10811-016-0849-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0849-9

Keywords

Search

Navigation