Pectinatella magnifica, an invasive bryozoan, might significantly affect ecosystem balance due to its massive occurrence in many areas in Europe and other parts of the world. Biological and chemical analyses are needed to get complete information about the impact of the animal on the environment. In this paper, we aimed to evaluate in vitro cytotoxic effects of five extracts prepared from P. magnifica using LDH assay on THP-1 cell line. Antimicrobial activities of extracts against 22 different bacterial strains were tested by microdilution method. Our study showed that all extracts tested, except aqueous portion, demonstrated LD50 values below 100 μg/mL, which indicates potential toxicity. The water extract of P. magnifica with LD50 value of 250 μg/mL also shows potentially harmful effects. Also, an environmental risk resulting from the presence and increasing biomass of potentially toxic benthic cyanobacteria in old colonies should not be underestimated. Toxicity of Pectinatella extracts could be partially caused by presence of Aeromonas species in material, since we found members of these genera as most abundant bacteria associated with P. magnifica. Furthermore, P. magnifica seems to be a promising source of certain antimicrobial agents. Its methanolic extract, hexane, and chloroform fractions possessed selective inhibitory effect on some potential pathogens and food spoiling bacteria in the range of MIC 0.5-10 mg/mL. Future effort should be made to isolate and characterize the content compounds derived from P. magnifica, which could help to identify the substance(s) responsible for the toxic effects of P. magnifica extracts.

Department of Biological Studies Faculty of Agriculture University of South Bohemia in České Budějovice Studentská 13 České Budějovice 37005 Czech Republic

Department of Botany Faculty of Science University of South Bohemia in České Budějovice Branišovská 31 České Budějovice 37005 Czech Republic

Department of Chemical Drugs Faculty of Pharmacy University of Veterinary and Pharmaceutical Sciences Palackého tř 1946 1 Brno 61242 Czech Republic

Department of Experimental Phycology and Ecotoxicology Institute of Botany Academy of Sciences of the Czech Republic Lidická 25 27 Brno 60200 Czech Republic

Department of Human Pharmacology and Toxicology Faculty of Pharmacy University of Veterinary and Pharmaceutical Sciences Palackého tř 1946 1 Brno 61242 Czech Republic

Department of Microbiology Nutrition and Dietetics Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 Prague 6 16521 Czech Republic

Department of Natural Drugs Faculty of Pharmacy University of Veterinary and Pharmaceutical Sciences Palackého tř 1946 1 Brno 61242 Czech Republic

Institute of Organic Chemistry and Biochemistry Academy of Sciences of the Czech Republic v v i Flemingovo nám 2 Prague 16610 Czech Republic

RECETOX Research Centre for Toxic Compounds in the Environment Faculty of Science Masaryk University Kamenice 753 5 Brno 60200 Czech Republic

See more in PubMed

Carroget P., Carroget L., Gruet Y., Baudet J., Dutertre M. Presence of colonies of the bryozoan Pectinatella magnifica Leidy 1851 in the Loire and the Nantes channel at Brest (Loire-Atlantique) Bull. Soc. Sci. Nat. Ouest. Fr. 2005;27:19–29.

Wood T.S. Bryozoans. In: Thorp J.H., Covich A.P., editors. Ecology and Classification of North American Freshwater Invertebrates. Academic Press; New York, NY, USA: 2001. pp. 505–525.

Kraepelin K. Zur Biologie und Fauna der Süßwasserbryozoen. Zool. Anz. 1884;7:319–321.

Balounová Z., Rajchard J., Švehla J., Šmahel L. The onset of invasion of bryozoan Pectinatella magnifica in South Bohemia (Czech Republic) Biologia. 2011;66:1091–1096. doi: 10.2478/s11756-011-0118-y. DOI

Rodriguez S., Vergon J.P. Pectinatella magnifica Leidy 1851 (Phylactolaemates), a species of bryozoa introduced in the north of Franche-Comté. Bull. Fr. Pech. Piscic. 2002;365/366:281–296. doi: 10.1051/kmae:2002036. DOI

Devin S., Bollache L., Noël P.Y., Beisel J.-N. Patterns of biological invasions in French freshwater systems by non-indigenous macroinvertebrates. Hydrobiologia. 2005;551:137–146. doi: 10.1007/s10750-005-4456-z. DOI

Balounová Z., Pechoušková E., Rajchard J., Joza V., Šinko J. World-Wide distribution of the Bryozoan Pectinatella magnifica (Leidy 1851) Eur. J. Environ. Sci. 2013;3:96–100.

Szekeres J., Akác A., Csányi B. First record of Pectinatella magnifica (Leidy 1851) in Hungary. Water Res. Manag. 2013;3:47–49.

Notteghem P. Évolution de la distribution de la Pectinatelle, Pectinatella magnifica (Leidy, 1851), Bryozoaire d’eau douce, en France et en Europe. Rev. Sci. Bourgogne-Nat. 2009;9/10:188–197.

Hyunbin J., Gea-Jae J., Myeoungseop B., Dong-Gyun H., Jung-Soo G., Ji-Yoon K., Jong-Yun C. Distribute pattern of Pectinatella magnifica (Leidy, 1851), an invasive species, in the Geum River and the Nakdong River, South Korea. J. Ecol. Environ. 2014;37:217–223.

Oda S. Pectinatella magnifica occurring in Lake Shoji, Japan. Proc. Jpn. Soc. Syst. Zool. 1974;10:31–39.

Brown C.J.D. A limnological study of certain fresh-water Polyzoa with special reference to their statoblasts. Trans. Am. Micros. Soc. 1933;52:271–314. doi: 10.2307/3222415. DOI

Seo J.E. Taxonomy of the freshwater bryozoans from Korea. Korean J. Syst. Zool. 1998;14:371–378.

Borg F. Moostierchen oder Bryozoen (Ectoprocten) In: Bischoff H., editor. Muschelinge oder Moluscocieda und Manteltiere oder Tunicata (Kamptozoa, Phoronidea, Bryozoa, Tunicata, Ascidiae). Die Tierwelt Deutschlands und der angrenzenden Meersteile nach ihren Merkmalen und nach ihrer Lebensweise. Jena; Gustav Fisher, Germany: 1930. pp. 25–142.

Prinsep M.R., Yao B., Nicholson B.K., Gordon D.P. The pterocellins, bioactive alkaloids from the marine bryozoan Pterocella vesiculosa. Phytochem. Rev. 2004;3:325–331. doi: 10.1007/s11101-004-6146-2. PubMed DOI

Kollar P., Rajchard J., Balounová Z., Pazourek J. Marine natural products: Bryostatins in preclinical and clinical studies. Pharm. Biol. 2014;52:237–242. doi: 10.3109/13880209.2013.804100. PubMed DOI

Dunlap W.C., Battershill C.N., Liptrot C.H., Coob R.E., Bourne D.G., Jaspars M., Long P.F., Newman D.J. Biomedicinals from the phytosymbionts of marine invertebrates: A molecular approach. Methods. 2007;42:358–376. doi: 10.1016/j.ymeth.2007.03.001. PubMed DOI

Figuerola B., Sla-Comorera L., Angulo-Preckler C., Vázquez J., Montes M.J., García-Aljaro C., Mercadé E., Blanch A.R., Avila C. Antimicrobial activity of Antarctic bryozoans: An ecological perspective with potential for clinical applications. Mar. Environ. Res. 2014;101:52–59. doi: 10.1016/j.marenvres.2014.09.001. PubMed DOI

Peters L., König M., Wright A.D., Pukall R., Stackebrandt E., Eberl L., Riede K. Secondary metabolites of Flustra foliacea and their influence on bacteria. Appl. Environ. Microbiol. 2003;69:3469–3475. doi: 10.1128/AEM.69.6.3469-3475.2003. PubMed DOI PMC

Walls J.T., Ritz D.A., Blackman A.J. Fouling, surface bacteria and antibacterial agents of four bryozoan species found in Tasmania, Australia. J. Exp. Mar. Biol. Ecol. 1993;169:1–13. doi: 10.1016/0022-0981(93)90039-Q. DOI

Sharp K.H., Davidson S.K., Haygood M.G. Localization of ‘Candidatus Endobugula Sertula’ and the bryostatins throughout the life cycle of the bryozoan Bugula neritina. ISME J. 2007;1:693–702. doi: 10.1038/ismej.2007.78. PubMed DOI

Molinski T.F., Dalisay D.S., Lievens S.L., Saludes J.P. Drug development from marine natural products. Nat. Rev. Drug Discov. 2009;8:69–85. doi: 10.1038/nrd2487. PubMed DOI

Paul V.J., Arthur K.E., Ritson-Williams R., Ross C., Sharp K. Chemical defenses: From Compounds to Communities. Biol. Bull. 2007;213:226–251. doi: 10.2307/25066642. PubMed DOI

Lopanik N., Gufson K.R., Lindquist N. Structure of bryostatin 20: A symbiont-produced chemical. Defense for larvae of the host bryozoan, Bugula neritina. J. Nat. Prod. 2004;67:1412–1414. doi: 10.1021/np040007k. PubMed DOI

Pejin B., Glamoclija J., Ciric A., Radotic K., Vajs V., Tesevic V., Hegedis A., Karaman I., Horvatovic M., Sokovic M. Antimicrobial activity of the freshwater bryozoan Hyalinella punctata (Hancock, 1850) Dig. J. Nanomater. Biostruct. 2012;7:1021–1026.

Pejin B., Ciric A., Horvatovic M., Jurca T., Glamoclija J., Nikolic M., Sokovic M. An insight into antimicrobial activity of the freshwater bryozoan Pectinatella magnifica. Nat. Prod. Res. 2016;30:1839–1843. doi: 10.1080/14786419.2015.1068773. PubMed DOI

Pejin B., Ciric A., Karaman I., Horvatovic M., Glamoclija J., Nikolic M., Sokovic M. In vitro antibiofilm activity of the freshwater bryozoan Hyalinella punctata: A case study of Pseudomonas aeruginosa PAO1. Nat. Prod. Res. 2016;30:1847–1850. doi: 10.1080/14786419.2015.1072714. PubMed DOI

Gad S.C. Alternatives to in vivo studies in toxicology. In: Ballantyne B., Marrs T., Syversen T., editors. General and Applied Toxicology. Volume 1. Grove’s Dictionaries Inc.; New York, NY, USA: 1999. p. 178.

Šetlíková I., Skácelová O., Šinko J., Rajchard J., Balounová Z. Ecology of Pectinatella magnifica and associated algae and cyanobacteria. Biologia. 2013;68:1136–1141. doi: 10.2478/s11756-013-0262-7. DOI

Shine R. The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q. Rev. Biol. 2010;85:253–291. doi: 10.1086/655116. PubMed DOI

Wood S.A., Smith F.M., Heath M.W., Palfroy T., Gaw S., Young R.G., Ryan K.G. Within-mat variability in anatoxin-a and homoanatoxin-a production among benthic Phormidium. (cyanobacteria) strains. Toxins. 2012;4:900–912. doi: 10.3390/toxins4100900. PubMed DOI PMC

Morse W. The chemical constitution of Pectinatella. Science (New York) 1930;71:265. doi: 10.1126/science.71.1836.265. PubMed DOI

Pazourek J., Šmejkal K., Kollár P., Rajchard J., Šinko J., Balounová Z., Vlková E., Salmonová H. Invasion of Pectinatella magnifica in Freshwater Resources of the Czech Republic. Int. J. Environ. Chem. Ecol. Geol. Geophys. Eng. 2016;111:278–285.

Fajkusová D., Pesko M., Keltošová S., Guo J., Oktabec Z., Vejsová M., Kollár P., Coffey A., Csollei J., Králová K., et al. Anti-Infective and herbicidal activity of N-substituted 2-aminobenzothiazoles. Bioorg. Med. Chem. 2012;20:7059–7068. doi: 10.1016/j.bmc.2012.10.007. PubMed DOI

Kos J., Zadražilová I., Peško M., Keltošová S., Tengler J., Goněc T., Bobáľ P., Kauerová T., Oravec M., Kollár P., et al. Antibacterial and herbicidal activity of ring-substituted 3-Hydroxynaphthalene-2-carboxanilides. Molecules. 2013;18:7977–7997. doi: 10.3390/molecules18077977. PubMed DOI PMC

Bhunia A.K. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis. Springer; New York, NY, USA: 2008. p. 134.

Silver A.C., Williams D., Faucher J., Horneman A.J., Gogarten J.P., Graf J. Complex evolutionary history of the Aeromonas veronii group revealed by host interaction and DNA sequence data. PLoS ONE. 2011;6:e16751. doi: 10.1371/journal.pone.0016751. PubMed DOI PMC

Sreedharan K., Philip R., Singh I.S. Characterization and virulence potential of phenotypically diverse Aeromonas veronii isolates recovered from moribund freshwater ornamental fishes of Kerala, India. Anton Leeuw. 2013;103:53–67. doi: 10.1007/s10482-012-9786-z. PubMed DOI

Heindl H., Wiese J., Thiel V., Imhoff J.F. Phylogenetic diversity and antimicrobial activities of bryozoan-associated bacteria isolated from Mediterranean and Baltic Sea habitats. Syst. Appl. Microbiol. 2010;33:94–104. doi: 10.1016/j.syapm.2009.12.002. PubMed DOI

Cronberg G., Annadotter H. Manual on Aquatic Cyanobacteria. A Photo Guide and a Synopsis of Their Toxicology. ISSHA; Copenhagen, Denmark: 2006. p. 106.

Glowacka J., Szefel-Markowska M., Waleron M., Łojkowska E., Waleron K. Detection and identification of potentially toxic cyanobacteria in Polish water bodies. Acta Biochim. Pol. 2011;58:321–333. PubMed

Quiblier C., Wood S., Echenique-Subiabre I., Heath M., Villeneuve A., Humbert J.-F. A review of current knowledge on toxic benthic freshwater cyanobacteria—Ecology, toxin production and risk management. Water Res. 2013;47:5464–5479. PubMed

Babica P., Kohoutek J., Bláha L., Adamovský O., Maršálek B. Evaluation of extraction approaches linked to ELISA and HPLC for analyses of microcystin-LR, -RR and -YR in freshwater sediments with different organic material contents. Anal. Bioanal. Chem. 2006;385:1545–1551. doi: 10.1007/s00216-006-0545-8. PubMed DOI

Faltermann S., Pretot R., Pernthaler J., Fent K. Comparative effects of nodularin and microcystin-LR in zebrafish: 1. Uptake by organic anion transporting polypeptide Oatp1d1 (Slco1d1) Aquat. Toxicol. 2016;171:69–76. doi: 10.1016/j.aquatox.2015.11.016. PubMed DOI

Chen L., Chen J., Zhang X.Z., Xie P. A review of reproductive toxicity of microcystins. J. Hazard. Mater. 2016;301:381–399. doi: 10.1016/j.jhazmat.2015.08.041. PubMed DOI

Guidelines for Drinking Water Quality. World Health Organization; Geneva, Switzerland: 2004. p. 407.

Kohoutek J., Adamovský O., Oravec M., Simek Z., Palíková M., Kopp R., Bláha L. LC-MS analyses of microcystins in fish tissues overestimate toxin levels-critical comparison with LC-MS/MS. Anal. Bioanal. Chem. 2010;398:1231–1237. doi: 10.1007/s00216-010-3860-z. PubMed DOI

Bláhová L., Babica P., Maršálková E., Maršálek B., Bláha L. Concentrations and seasonal trends of extracellular microcystins in freshwaters of the Czech Republic—Results of the national monitoring program. Clean-Soil Air Water. 2007;35:348–354. doi: 10.1002/clen.200700010. DOI

Bláhova L., Babica P., Adamovský O., Kohoutek J., Maršálek B., Bláha L. Analyses of cyanobacterial toxins (microcystins, cylindrospermopsin) in the reservoirs of the Czech Republic and evaluation of health risks. Environ. Chem. Lett. 2008;6:223–227. doi: 10.1007/s10311-007-0126-x. DOI

Jančula D., Straková L., Sadílek J., Maršálek B., Babica P. Survey of cyanobacterial toxins in Czech water reservoirs - the first observation of neurotoxic saxitoxins. Environ. Sci. Pollut. Res. 2014;21:8006–8015. doi: 10.1007/s11356-014-2699-9. PubMed DOI

Carey C.C., Haney J.F., Cottingham K.L. First report of microcystin-LR in the cyanobacterium Gloeotrichia echinulata. Environ. Toxicol. 2007;22:337–339. doi: 10.1002/tox.20245. PubMed DOI

Richardson L.L., Sekar R., Myers J.L., Gantar M., Voss J.D., Kaczmarsky L., Remily E.R., Boyer G.L., Zimba P.V. The presence of the cyanobacterial toxin microcystin in black band disease of corals. FEMS Microbiol. Lett. 2007;272:182–187. doi: 10.1111/j.1574-6968.2007.00751.x. PubMed DOI

Kaasalainen U., Fewer D.P., Jokela J., Wahlsten M., Sivonen K., Rikkinen J. Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis. Proc. Natl. Acad. Sci. USA. 2012;109:5886–5891. doi: 10.1073/pnas.1200279109. PubMed DOI PMC

Bellinger B.J., Hagerthey S.E. Presence and Diversity of Algal Toxins in Subtropical Peatland Periphyton: the Florida Everglades, USA. J. Phycol. 2010;46:674–678. doi: 10.1111/j.1529-8817.2010.00832.x. DOI

Testai E., Buratti F.M., Funari E., Manganelli M., Vichi S., Arnich N., Biré R., Fessard V., Sialehaamoa A. Review and analysis of occurrence, exposure and toxicity of cyanobacteria toxins in food. EFSA Support. Publ. 2016;13 doi: 10.2903/sp.efsa.2016.EN-998. DOI

Ibelings B.W., Havens K.E. Cyanobacterial toxins: A qualitative meta-analysis of concentrations, dosage and effects in freshwater, estuarine and marine biota. In: Hudnell H.K., editor. Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs. Springer; Berlin, Germany: 2008. pp. 675–732. PubMed

Sieniawska E., Baj T., Dudka J., Gieroba R., Swiatek L., Rajtar B., Glowniak K., Polz-Dacewicz M. Cytotoxicity, antioxidant activity and an effect on CYP3A4 and CYP2D6 of Mutellina purpurea L. extracts. Food Chem. Toxicol. 2013;52:188–192. doi: 10.1016/j.fct.2012.11.017. PubMed DOI

Kmeť V., Drugdová Z. Antimicrobial susceptibility of microflora from ovine cheese. Folia Microbiol. 2012;57:291–293. doi: 10.1007/s12223-012-0128-3. PubMed DOI