{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T01:09:18Z","timestamp":1760231358096,"version":"build-2065373602"},"reference-count":31,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T00:00:00Z","timestamp":1663200000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"FCT\u2014Foundation for Science and Technology","award":["UIDB\/04423\/2020","UIDP\/04423\/2020","PTDC\/AAG-GLO\/2317\/2014 (POCI-01-0145-FEDER-016799)","PTDC\/CTA-AMB\/31774\/2017 (POCI-01-0145-FEDER\/031774\/2017)","SFRH\/BPD\/122909\/2016"],"award-info":[{"award-number":["UIDB\/04423\/2020","UIDP\/04423\/2020","PTDC\/AAG-GLO\/2317\/2014 (POCI-01-0145-FEDER-016799)","PTDC\/CTA-AMB\/31774\/2017 (POCI-01-0145-FEDER\/031774\/2017)","SFRH\/BPD\/122909\/2016"]}]},{"name":"FCT projects","award":["UIDB\/04423\/2020","UIDP\/04423\/2020","PTDC\/AAG-GLO\/2317\/2014 (POCI-01-0145-FEDER-016799)","PTDC\/CTA-AMB\/31774\/2017 (POCI-01-0145-FEDER\/031774\/2017)","SFRH\/BPD\/122909\/2016"],"award-info":[{"award-number":["UIDB\/04423\/2020","UIDP\/04423\/2020","PTDC\/AAG-GLO\/2317\/2014 (POCI-01-0145-FEDER-016799)","PTDC\/CTA-AMB\/31774\/2017 (POCI-01-0145-FEDER\/031774\/2017)","SFRH\/BPD\/122909\/2016"]}]},{"name":"FCT","award":["UIDB\/04423\/2020","UIDP\/04423\/2020","PTDC\/AAG-GLO\/2317\/2014 (POCI-01-0145-FEDER-016799)","PTDC\/CTA-AMB\/31774\/2017 (POCI-01-0145-FEDER\/031774\/2017)","SFRH\/BPD\/122909\/2016"],"award-info":[{"award-number":["UIDB\/04423\/2020","UIDP\/04423\/2020","PTDC\/AAG-GLO\/2317\/2014 (POCI-01-0145-FEDER-016799)","PTDC\/CTA-AMB\/31774\/2017 (POCI-01-0145-FEDER\/031774\/2017)","SFRH\/BPD\/122909\/2016"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>Cyanobacteria are a bloom-forming ancient group of photosynthetic prokaryotes. A rise in temperature is a major contributor to its massive proliferation, namely on freshwater ecosystems, with social and economic impacts. Thus, reliable and cost-effective tools can permit the fast surveillance and assessment of temperature effects on potentially toxic cyanobacteria distribution and impacts. The occurrence of three potentially toxic cyanobacteria species was assessed on seven sampling points across three sampling years. Moreover, the association between the occurrence of those cyanobacteria species with climate change events was addressed. Here, we combined molecular and statistical methods to study the impacts of temperature on the occurrence of three globally occurring cyanotoxin-producing cyanobacteria species\u2014Microcystis aeruginosa (microcystins), Raphidiopsis raciborskii (cylindrospermopsins and saxitoxins) and Planktothrix agardhii (microcystins and saxitoxins). Samples were collected on seven European temperate freshwater systems located on the North and Centre regions of Portugal, across three distinct sampling years with distinct ranges of air temperature. Data support that M. aeruginosa is still a common inhabitant of Portuguese freshwater ecosystems and a new trend was found on R. raciborskii recent invasion and establishment on the colder north ecosystems of Portugal. Additionally, the highest frequency of detection of both cyanobacteria was associated with warmer years. P. agardhii also revealed a new trend, being reported for the first time on North and Centre Regions of Portugal, however with no statistical relation with air temperature, demonstrating a higher ecological fitness. Distinct profiles of the statistical analysis on the three tested cyanobacteria species contribute to deepen the studies on other species as well as of our analyzed species on a global level. This assessment may help to anticipate possible repercussions on water quality and public health due to most probable alterations on cyanotoxins profile given the ecological fitness established among air temperature and PCR detection of potentially toxic cyanobacteria.<\/jats:p>","DOI":"10.3390\/toxins14090638","type":"journal-article","created":{"date-parts":[[2022,9,16]],"date-time":"2022-09-16T03:48:04Z","timestamp":1663300084000},"page":"638","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Statistical Inferences Applying Non-Parametric Data on Cyanobacterial Investigations: Contributions to Water Quality and New Trends under Global Changes on Portuguese Freshwater Ecosystems"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0860-2949","authenticated-orcid":false,"given":"Cristiana","family":"Moreira","sequence":"first","affiliation":[{"name":"CIIMAR\/CIMAR\u2014Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450\u2013208 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5331-2660","authenticated-orcid":false,"given":"Ana","family":"Matos","sequence":"additional","affiliation":[{"name":"CIIMAR\/CIMAR\u2014Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450\u2013208 Porto, Portugal"},{"name":"Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal"}]},{"given":"Aldo","family":"Barreiro","sequence":"additional","affiliation":[{"name":"CIIMAR\/CIMAR\u2014Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450\u2013208 Porto, Portugal"}]},{"given":"Cid\u00e1lia","family":"Gomes","sequence":"additional","affiliation":[{"name":"CIIMAR\/CIMAR\u2014Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450\u2013208 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3585-2417","authenticated-orcid":false,"given":"Vitor","family":"Vasconcelos","sequence":"additional","affiliation":[{"name":"CIIMAR\/CIMAR\u2014Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450\u2013208 Porto, Portugal"},{"name":"Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1328-1732","authenticated-orcid":false,"given":"Agostinho","family":"Antunes","sequence":"additional","affiliation":[{"name":"CIIMAR\/CIMAR\u2014Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leix\u00f5es, Av. General Norton de Matos, s\/n, 4450\u2013208 Porto, Portugal"},{"name":"Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1038\/nature02260","article-title":"Dating the rise of atmospheric oxygen","volume":"427","author":"Bekker","year":"2004","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1791","DOI":"10.1073\/pnas.1209927110","article-title":"Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event","volume":"110","author":"Schirrmeister","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2036","DOI":"10.3390\/md12042036","article-title":"Cyanobacteria from Terrestrial and Marine Sources Contain Apoptogens Able to Overcome Chemoresistance in Acute Myeloid Leukemia Cells","volume":"12","author":"Liu","year":"2014","journal-title":"Mar. Drugs"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3390\/ijerph2005010043","article-title":"Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water","volume":"2","author":"Falconer","year":"2005","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.1080\/20018091095087","article-title":"Health Effects of Toxin-Producing Cyanobacteria: \u201cThe CyanoHABs\u201d","volume":"7","author":"Carmichael","year":"2001","journal-title":"Hum. Ecol. Risk Assess. An Int. J."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"5074","DOI":"10.1073\/pnas.0501526102","article-title":"Diverse taxa of cyanobacteria produce -N-methylamino-L-alanine, a neurotoxic amino acid","volume":"102","author":"Cox","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1002\/mnfr.200500162","article-title":"Cyanobacterial toxins\u2014Occurrence, biosynthesis and impact on human affairs","volume":"50","author":"Dittmann","year":"2006","journal-title":"Mol. Nutr. Food Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1056\/NEJM199803263381304","article-title":"Liver Failure and Death after Exposure to Microcystins at a Hemodialysis Center in Brazil","volume":"338","author":"Jochimsen","year":"1998","journal-title":"N. Engl. J. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1292","DOI":"10.1128\/aem.50.5.1292-1295.1985","article-title":"Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir","volume":"50","author":"Hawkins","year":"1985","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.1016\/S0041-0101(99)00080-X","article-title":"The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil","volume":"37","author":"Lagos","year":"1999","journal-title":"Toxicon"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1007\/s002530100810","article-title":"Molecular biology of peptide and polyketide biosynthesis in cyanobacteria","volume":"57","author":"Dittmann","year":"2001","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1111\/j.1574-6941.2011.01242.x","article-title":"What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii?","volume":"79","author":"Bonilla","year":"2012","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1128\/AEM.66.1.332-338.2000","article-title":"Molecular Characterization of the Toxic Cyanobacterium Cylindrospermopsis raciborskii and Design of a Species-Specific PCR","volume":"66","author":"Wilson","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3695","DOI":"10.1099\/mic.0.2007\/010645-0","article-title":"Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa","volume":"153","author":"Tanabe","year":"2007","journal-title":"Microbiology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1007\/s00203-012-0809-y","article-title":"Species-specific real-time PCR cell number quantification of the bloom-forming cyanobacterium Planktothrix agardhii","volume":"194","author":"Churro","year":"2012","journal-title":"Arch. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"45","DOI":"10.23818\/limn.20.05","article-title":"Cyanobacteria toxins: Diversity and Ecological Effects","volume":"20","author":"Vasconcelos","year":"2001","journal-title":"Limnetica"},{"key":"ref_17","unstructured":"Caetano, S. (2015). Toxicity Risks Linked to Cyanobacteria Blooms in Southern Portugal Reservoirs. [Ph.D. Thesis, University of Algarve]."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.toxicon.2008.11.016","article-title":"Toxicity of cylindrospermopsin, and other apparent metabolites from Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum, to the zebrafish (Danio rerio) embryo","volume":"53","author":"Berry","year":"2009","journal-title":"Toxicon"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Churro, C., Azevedo, J., Vasconcelos, V., and Silva, A. (2017). Detection of a Planktothrix agardhii Bloom in Portuguese Marine Coastal Waters. Toxins, 9.","DOI":"10.3390\/toxins9120391"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1007\/s11274-016-2063-y","article-title":"Genetic characterization of Microcystis aeruginosa isolates from Portuguese freshwater systems","volume":"32","author":"Moreira","year":"2016","journal-title":"World J. Microbiol. Biotechnol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"van Gremberghe, I., Leliaert, F., Mergeay, J., Vanormelingen, P., Van der Gucht, K., Debeer, A.-E., Lacerot, G., De Meester, L., and Vyverman, W. (2011). Lack of Phylogeographic Structure in the Freshwater Cyanobacterium Microcystis aeruginosa Suggests Global Dispersal. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0019561"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.toxicon.2017.02.024","article-title":"First occurrence of cylindrospermopsin in Portugal: A contribution to its continuous global dispersal","volume":"130","author":"Moreira","year":"2017","journal-title":"Toxicon"},{"key":"ref_23","first-page":"563","article-title":"Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: Worldwide distribution and review of its ecology","volume":"107","year":"1997","journal-title":"Arch. Hydrobiol. Suppl. Monogr. Beitr."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1128\/AEM.71.2.1097-1100.2005","article-title":"Genetic Diversity of Cylindrospermopsis Strains (Cyanobacteria) Isolated from Four Continents","volume":"71","author":"Gugger","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","unstructured":"Morais, J. (2009). Avalia\u00e7\u00e3o do Risco de Ocorr\u00eancia de Cianobact\u00e9rias T\u00f3xicas nos Lagos do Parque da Cidade do Porto. [Master\u2019s Thesis, University of Porto]."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1080\/09670262.2010.492916","article-title":"The ecology of the invasive cyanobacterium Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) in two hypereutrophic lakes dominated by Planktothrix agardhii (Oscillatoriales, Cyanophyta)","volume":"45","author":"Stefaniak","year":"2010","journal-title":"Eur. J. Phycol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1590\/S1519-69842008000300004","article-title":"Phytoplankton community and physical-chemical characteristics of water in the public reservoir of Cruzeta, RN, Brazil","volume":"68","author":"Chellappa","year":"2008","journal-title":"Braz. J. Biol."},{"key":"ref_28","first-page":"5","article-title":"Instructions for preparation of modified nutrient solution Z8 for algae","volume":"11","author":"Kotai","year":"1972","journal-title":"Nor. Inst. Water Res. Oslo"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1099\/00207713-47-3-693","article-title":"rRNA Sequences and Evolutionary Relationships among Toxic and Nontoxic Cyanobacteria of the Genus Microcystis","volume":"47","author":"Neilan","year":"1997","journal-title":"Int. J. Syst. Bacteriol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1111\/j.1462-2920.2005.00717.x","article-title":"Diversity within cyanobacterial mat communities in variable salinity meltwater ponds of McMurdo Ice Shelf, Antarctica","volume":"7","author":"Jungblut","year":"2005","journal-title":"Environ. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1007\/s00203-003-0605-9","article-title":"PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera","volume":"180","author":"Hisbergues","year":"2003","journal-title":"Arch. Microbiol."}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/14\/9\/638\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:32:15Z","timestamp":1760142735000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/14\/9\/638"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,15]]},"references-count":31,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["toxins14090638"],"URL":"https:\/\/doi.org\/10.3390\/toxins14090638","relation":{},"ISSN":["2072-6651"],"issn-type":[{"type":"electronic","value":"2072-6651"}],"subject":[],"published":{"date-parts":[[2022,9,15]]}}}