DNA barcoding approach to characterize microalgae isolated from freshwater systems in Ecuador

References

• Guiry MD. How many species of algae are there? J Phycol. 2012;48(5):1057–1063.
   PubMed Web of Science ®Google Scholar
• Hollingsworth PM. Refining the DNA barcode for land plants. Proc Natl Acad Sci U S A. 2011;108(49):19451–19452.
   PubMed Web of Science ®Google Scholar
• Hubert N, Hanner R, Holm E, et al. Identifying Canadian freshwater fishes through DNA barcodes. PLoS One. 2008;3(6):e2490.
   PubMed Web of Science ®Google Scholar
• Torres MA, Barros MP, Campos SCG, et al. Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf. 2008;71(1):1–15.
   PubMed Web of Science ®Google Scholar
• Omar WMW. Perspectives on the use of algae as biological indicators for monitoring and protecting aquatic environments, with special reference to Malaysian freshwater ecosystems. Trop Life Sci Res. 2010;21(2):51–67.
   PubMedGoogle Scholar
• Al-Haj L, Lui Y, Abed R, et al. Cyanobacteria as chassis for industrial biotechnology: progress and prospects. Life. 2016;6(4):42.
   Google Scholar
• Mišurcová L, Škrovánková S, Samek D, et al. Health benefits of Algal Polysaccharides in human nutrition. Adv Food Nutr Res. 2012; 66:75–145. Elsevier Inc.
   Google Scholar
• Khanna N, Lindblad P. Cyanobacterial hydrogenases and hydrogen metabolism revisited: recent progress and future prospects. Int J Mol Sci. 2015;16(12):10537–10561.
   PubMedGoogle Scholar
• Zehr JP. Nitrogen fixation by marine cyanobacteria. Trends Microbiol. 2011;19(4):162–173.
   PubMed Web of Science ®Google Scholar
• Jagielski T, Bakuła Z, Gawor J, et al. The genus Prototheca (Trebouxiophyceae, Chlorophyta) revisited: implications from molecular taxonomic studies. Algal Res. 2019;43:101639.
   Google Scholar
• Guamán C, Nory B, Romero PG. Catálogo de microalgas y cianobacterias de agua dulce del Ecuador. Quito: Laboratorio de Biotecnología Energética; 2016.
   Google Scholar
• Nakayama T, Watanabe S, Mitsui K, et al. The phylogenetic relationship between the Chlamydomonadales and Chlorococcales inferred from 18SrDNA sequence data. Phycol Res. 1996;44(1):47–55.
   Google Scholar
• Škaloud P, Neustupa J, Radochová B, et al. Confocal microscopy of chloroplast morphology and ontogeny in three strains of Dictyochloropsis (Trebouxiophyceae, Chlorophyta). Phycologia. 2005;44(3):261–269.
   Web of Science ®Google Scholar
• Komárek J, Kaštovský J, Mareš J, et al. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia. 2014;86:295–335.
   Web of Science ®Google Scholar
• Gugger M, Lyra C, Henriksen P, et al. Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon. Int J Syst Evol Microbiol. 2002;52(Pt 5):1867–1880.
   PubMedGoogle Scholar
• Lehtimäki J, Lyra C, Suomalainen S, et al. Characterization of Nodularia strains, cyanobacteria from brackish waters, by genotypic and phenotypic methods. Int J Syst Evol Microbiol. 2000;50(3):1043–1053.
   PubMedGoogle Scholar
• Manoylov KM, Graham L. Taxonomic identification of algae (morphological and molecular): species concepts, methodologies, and their implications for ecological bioassessment. J Phycol. 2014;50(3):409–424. Graham L, editor.
   PubMed Web of Science ®Google Scholar
• Hall JD, Fučíková K, Lo C, et al. An assessment of proposed DNA barcodes in freshwater green algae. Cryptogam Algol. 2010;31:529–555.
   Web of Science ®Google Scholar
• Alemzadeh E, Haddad R, Ahmadi A. Phytoplanktons and DNA barcoding : characterization and molecular analysis of phytoplanktons on the Persian Gulf. Iran J Microbiol. 2014;6(4):296–302.
   PubMedGoogle Scholar
• Bock C, Krienitz L, Pröschold T. Taxonomic reassessment of the genus Chlorella (Trebouxiophyceae) using molecular signatures (barcodes), including description of seven new species. Fottea. 2011;11(2):293–312.
   Web of Science ®Google Scholar
• Esling P, Lejzerowicz F, Pawlowski J. Accurate multiplexing and filtering for high-throughput amplicon-sequencing. Nucleic Acids Res. 2015;43(5):2513–2524.
   PubMed Web of Science ®Google Scholar
• Pawlowski J, Holzmann M. A plea for DNA barcoding of foraminifera. J Foraminiferal Res. 2014;44(1):62–67.
   Web of Science ®Google Scholar
• Hebert P, Cywinska A, Ball S, et al. Biological identifications through DNA barcodes. Proc Biol Sci. 2003;270(1512):313–321.
   PubMed Web of Science ®Google Scholar
• Hebert PDN, Ratnasingham S, Dewaard JR. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B. 2003;270(suppl_1):S96–S99.
   PubMedGoogle Scholar
• Schloss PD, Handelsman J, Relman D. Toward a census of bacteria in soil. PLoS Comput Biol. 2006;2(7):0786–0793.
   Web of Science ®Google Scholar
• Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rDNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol Microbiol Soc. 1994;44(4):846–849.
   Web of Science ®Google Scholar
• Blaxter ML, Godfray HCJ, Knapp S. The promise of a DNA taxonomy. Philos Trans R Soc B Biol Sci. 2004;359(1444):669–679.
   PubMed Web of Science ®Google Scholar
• Pawlowski J, Lejzerowicz F, Apotheloz-Perret-Gentil L, et al. Protist metabarcoding and environmental biomonitoring: time for change. Eur J Protistol. 2016;55:12–25.
   PubMed Web of Science ®Google Scholar
• Pernice MC, Logares R, Guillou L, et al. General patterns of diversity in major marine Microeukaryote Lineages. PLoS One. 2013;8(2):e57170.
   PubMed Web of Science ®Google Scholar
• DeSalle R, Goldstein P. Review and interpretation of trends in DNA barcoding. Front Ecol Evol. 2019;7:1–11.
   Web of Science ®Google Scholar
• Pawlowski J, Audic S, Adl S, et al. CBOL Protist Working Group: barcoding Eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol. 2012;10(11):e1001419.
   PubMed Web of Science ®Google Scholar
• Buchheim MA, Keller A, Koetschan C, et al. Internal transcribed spacer 2 (nu ITS2 rDNA) sequence-structure phylogenetics: towards an automated reconstruction of the green algal tree of life. PLoS One. 2011;6(2):e16931.
   PubMed Web of Science ®Google Scholar
• Fawley MW, Fawley KP, Buchheim MA. Molecular diversity among communities of freshwater microchlorophytes. Microb Ecol. 2004;48(4):489–499.
   PubMed Web of Science ®Google Scholar
• Medlin LK, Metfies K, Mehl H, et al. Picoeukaryotic plankton diversity at the Helgoland time series site as assessed by three molecular methods. Microb Ecol. 2006;52(1):53–71.
   PubMed Web of Science ®Google Scholar
• Not F, Del Campo J, Balagué V, et al. New insights into the diversity of Marine Picoeukaryotes. PLoS One. 2009;4(9):e7143.
   PubMed Web of Science ®Google Scholar
• Hadziavdic K, Lekang K, Lanzen A, et al. Characterization of the 18S rDNA gene for designing universal Eukaryote specific primers. PLoS One. 2014;9(2):e87624.
   PubMed Web of Science ®Google Scholar
• Zimmermann J, Jahn R, Gemeinholzer B. Barcoding diatoms: evaluation of the V4 subregion on the 18S rDNA gene, including new primers and protocols. Org Divers Evol. 2011;11(3):173–192.
   Web of Science ®Google Scholar
• Hadi SIIA, Santana H, Brunale PPM, et al. DNA barcoding green microalgae isolated from neotropical Inland waters. PLoS One. 2016;11(2):e0149284.
   PubMed Web of Science ®Google Scholar
• Lortou U, Gkelis S. Polyphasic taxonomy of green algae strains isolated from Mediterranean freshwaters. Biol Res-Thessaloniki. 2019;26(1):11.
   PubMed Web of Science ®Google Scholar
• Dadheech PK, Glöckner G, Casper P, et al. Cyanobacterial diversity in the hot spring, pelagic and benthic habitats of a tropical soda lake. FEMS Microbiol Ecol. 2013;85(2):389–401.
   PubMed Web of Science ®Google Scholar
• Rosselló-Mora R. Updating prokaryotic taxonomy. J Bacteriol. 2005;187(18):6255–6257.
   PubMed Web of Science ®Google Scholar
• Boyer SL, Flechtner VR, Johansen JR. Is the 16S-23S rDNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol. 2001;18(6):1057–1069.
   PubMed Web of Science ®Google Scholar
• Otsuka S, Suda S, Li R, et al. Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol Lett. 1999;172(1):15–21.
   PubMed Web of Science ®Google Scholar
• Rocap G, Distel DL, Waterbury JB, et al. Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol. 2002;68(3):1180–1191.
   PubMed Web of Science ®Google Scholar
• Wilmotte A. Molecular evolution and taxonomy of the Cyanobacteria. In: D.A. B, editor. Mol Biol Cyanobacteria. Dordrecht: Springer Netherlands; 1994. p. 1–25.
   Google Scholar
• Wilmotte A, Neefs JM, De Wachter R. Evolutionary affiliation of the marine nitrogen-fixing cyanobacterium Trichodesmium sp. strain NIBB 1067, derived by 16S ribosomal RNA sequence analysis. Microbiology. 1994;140(8):2159–2164.
   PubMedGoogle Scholar
• Mikhailyuk T, Glaser K, Tsarenko P, et al. Composition of biological soil crusts from sand dunes of the Baltic Sea coast in the context of an integrative approach to the taxonomy of microalgae and cyanobacteria. Eur J Phycol. 2019;54(3):263–290.
   Web of Science ®Google Scholar
• Ríos-Touma B, Holzenthal RW, Huisman J, et al. Diversity and distribution of the Caddisflies (Insecta: trichoptera) of Ecuador. Peer J. 2017;5:e2851.
   PubMed Web of Science ®Google Scholar
• Gunkel G, Beulker C. Limnology of the crater Lake Cuicocha, Ecuador, a cold water tropical lake. Int Rev Hydrobiol. 2009;94(1):103–125.
   Web of Science ®Google Scholar
• Andersen RA. Algal culturing techniques. London: Elsevier Academic Press; 2005.
   Google Scholar
• Bellinger EG, Sigee DC. Freshwater algae: identification, enumeration and use as bioindicators. Wileyblackwell; United States of America, 2015.
   Google Scholar
• Serediak N, Huynh M. Algae identification lab guide : accompanying manual to the algae identification field guide. Canada. CA and A-F, editor. Ottawa: Agriculture and Agri-Food Canada; 2011.
   Google Scholar
• Guiry MD, Guiry GM. AlgaeBase. Galway: World-wide electronic publication, National University of Ireland. https://www.algaebase.org; searched on 01 November 2020.
   Google Scholar
• Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–1549.
   PubMed Web of Science ®Google Scholar
• Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797.
   PubMed Web of Science ®Google Scholar
• Mareš J, Hrouzek P, Kaňa R, et al. The primitive Thylakoid-Less Cyanobacterium Gloeobacter is a Common Rock-Dwelling Organism. PLoS One. 2013;8(6):e66323.
   PubMed Web of Science ®Google Scholar
• Mora D, Abarca N, Proft S, et al. Morphology and metabarcoding: a test with stream diatoms from Mexico highlights the complementarity of identification methods. Freshw Sci. 2019;38(3):448–464.
   Web of Science ®Google Scholar
• Zimmermann J, Abarca N, Enk N, et al. Taxonomic reference libraries for environmental barcoding: a best practice example from diatom research. PLoS One. 2014;9(9):e114758.
   Web of Science ®Google Scholar
• Zimmermann J, Glöckner G, Jahn R, et al. Metabarcoding vs. morphological identification to assess diatom diversity in environmental studies. Mol Ecol Resour. 2015;15(3):526–542.
   PubMed Web of Science ®Google Scholar
• Correia N, Pereira H, Silva JT, et al. Isolation, identification and biotechnological applications of a novel, robust, free-living Chlorococcum (Oophila) amblystomatis strain isolated from a local pond. Appl Sci. 2020;10(9):3040.
   Google Scholar
• Hoshina R, Fujiwara Y. Molecular characterization of Chlorella cultures of the National Institute for Environmental Studies culture collection with description of Micractinium inermum sp. nov., Didymogenes sphaerica sp. nov., and Didymogenes soliella sp. nov. (Chlorellaceae, Tr.). Phycol Res. 2013;61:124–132.
   Web of Science ®Google Scholar
• Leliaert F, Verbruggen H, Vanormelingen P, et al. DNA-based species delimitation in algae. Eur J Phycol. 2014;49(2):179–196.
   Web of Science ®Google Scholar
• Lee SR, Oak JH, Chung IK, et al. Effective molecular examination of eukaryotic plankton species diversity in environmental seawater using environmental PCR, PCR-RFLP, and sequencing. J Appl Phycol. 2010;22(6):699–707.
   Web of Science ®Google Scholar
• Wang Q, Song H, Liu X, et al. Morphology and molecular phylogeny of coccoid green algae Coelastrella sensu lato (Scenedesmaceae, Sphaeropeales), including the description of three new species and two new varieties. J Phycol. 2019;55(6):1290–1305.
   PubMed Web of Science ®Google Scholar
• Ancona-Canché K, López-Adrián S, Espinosa-Aguilar M, et al. Molecular phylogeny and morphologic data of strains of the genus Coelastrella (Chlorophyta, Scenedesmaceae) from a tropical region in North America (Yucatan Peninsula). Bot Sci. 2017;95(3):527–537.
   Web of Science ®Google Scholar
• Hegewald E, Wolf M. Phylogenetic relationships of Scenedesmus and Acutodesmus (Chlorophyta, Chlorophyceae) as inferred from 18S rDNA and ITS-2 sequence comparisons. Plant Syst Evol. 2003;241(3–4):185–191.
   Web of Science ®Google Scholar
• Zou S, Fei C, Wang C, et al. How DNA barcoding can be more effective in microalgae identification: a case of cryptic diversity revelation in Scenedesmus (Chlorophyceae). Sci Rep. 2016;6(1):1–13.
   PubMedGoogle Scholar
• Krienitz L, Hegewald EH, Hepperle D, et al. Phylogenetic relationship of Chlorella and Parachlorella gen. nov. (Chlorophyta, Trebouxiophyceae). Phycologia. 2004;43(5):529–542.
   Web of Science ®Google Scholar
• Sciuto K, Lewis LA, Verleyen E, et al. Chodatodesmus australis sp. nov. (Scenedesmaceae, Chlorophyta) from Antarctica, with the emended description of the genus Chodatodesmus, and circumscription of Flechtneria rotunda gen. et sp. nov. J Phycol. 2015;51(6):1172–1188.
   PubMed Web of Science ®Google Scholar
• Eliáš M, Němcová Y, Škaloud P, et al. Hylodesmus singaporensis gen. et sp. nov., a new autosporic subaerial green alga (Scenedesmaceae, Chlorophyta) from Singapore. Int J Syst Evol Microbiol. 2010;60(5):1224–1235.
   PubMedGoogle Scholar
• Hegewald E. A new subdivision of the genus Scenedesmus Meyen. Nov Hedwigia. 1978;30(1–4):343–376.
   Google Scholar
• An SS, Friedl T, Hegewald E. Phylogenetic relationships of Scenedesmus and Scenedesmus-like Coccoid Green Algae as Inferred from ITS-2 rDNA Sequence Comparisons. Plant Biol. 1999;1(4):418–428.
   Web of Science ®Google Scholar
• Huss VAR, Frank C, Hartmann EC, et al. Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). J Phycol. 1999;35(3):587–598.
   Web of Science ®Google Scholar
• Darienko T, Pröschold T. The genus Jaagichlorella Reisigl (Trebouxiophyceae, Chlorophyta) and its close relatives: an evolutionary puzzle. Phytotaxa. 2019;388(1):047–068.
   Web of Science ®Google Scholar
• Cadillo-Quiroz H, Didelot X, Held NL, et al. Patterns of gene flow define species of Thermophilic Archaea. PLOS Biol. 2012;10(2):e1001265.
   PubMed Web of Science ®Google Scholar
• Eckert EM, Fontaneto D, Coci M, et al. Does a barcoding gap exist in prokaryotes? Evidences from species delimitation in cyanobacteria. Life. 2015;5(1):50–64.
   Google Scholar
• Schleifer KH. Classification of bacteria and archaea: past, present and future. Syst Appl Microbiol. 2009;32(8):533–542. Dec 1.
   PubMed Web of Science ®Google Scholar
• Valério E, Chambel L, Paulino S, et al. Molecular identification, typing and traceability of cyanobacteria from freshwater reservoirs. Microbiology. 2009;155(2):642–656.
   PubMedGoogle Scholar
• Komárek J, Anagnostidis K. Modern approach to the classification system of Cyanophytes 4 - Nostocales. Algol Stud für Hydrobiol. 1989; Suppl Vol. 56:247–345.
   Google Scholar
• Moreira C, Vasconcelos V, Antunes A. Genetic characterization of Microcystis aeruginosa isolates from Portuguese freshwater systems. World J Microbiol Biotechnol. 2016;32(7):32.
   PubMed Web of Science ®Google Scholar
• Kurobe T, Lehman PW, Hammock BG, et al. Biodiversity of cyanobacteria and other aquatic microorganisms across a freshwater to brackish water gradient determined by shotgun metagenomic sequencing analysis in the San Francisco Estuary, USA. PLoS One. 2018;13(9):1–20.
   Web of Science ®Google Scholar
• Yoshida M, Yoshida T, Satomi M, et al. Intra-specific phenotypic and genotypic variation in toxic cyanobacterial Microcystis strains. J Appl Microbiol. 2008;105(2):407–415.
   PubMed Web of Science ®Google Scholar
• Singh R, Parihar P, Singh M, et al. Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol. 2017;8:1–37.
   PubMed Web of Science ®Google Scholar
• Włodarczyk A, Selão TT, Norling B, et al. Newly discovered Synechococcus sp. PCC 11901 is a robust cyanobacterial strain for high biomass production. Commun Biol. 2020;3(1):215.
   PubMed Web of Science ®Google Scholar
• Vela-garcía N, Guamán-Burneo MC, González-Romero NP. Efficient bioremediation from metallurgical effluents through the use of microalgae isolated from the Amazonic and highlands of Ecuador. Rev Int Contam Ambie. 2019;35(4):917–929.
   Web of Science ®Google Scholar
• Hodač L, Hodač H, Hallmann C, et al. Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol Ecol. 2016;92(8):122.
   Web of Science ®Google Scholar
• Aray-Andrade MM, Uyaguari-Diaz MI, Rafael Bermú Dez J, et al. Short-term deleterious effects of standard isolation and cultivation methods on new tropical freshwater microalgae strains dist. PeerJ. 2018;6:e5143.
   PubMed Web of Science ®Google Scholar
• Ballesteros I, Castillejo P, Haro AP, et al. Genetic barcoding of Ecuadorian epilithic diatom species suitable as water quality bioindicators. C R Biol. 2020;343(1):41–52.
   PubMed Web of Science ®Google Scholar
• Chagnon PL, Magain N, Miadlikowska J, et al. Strong specificity and network modularity at a very fine phylogenetic scale in the lichen genus Peltigera. Oecologia. 2018;187(3):767–782.
   PubMed Web of Science ®Google Scholar
• Nübel U, Muyzer G, Garcia-pichel F, et al. PCR primers to amplify 16S rDNA genes from cyanobacteria PCR primers to amplify 16S rDNA genes from Cyanobacteria. Microbiology. 1997;63:3327–3332.
   Web of Science ®Google Scholar
• Visco JA, Apothéloz-Perret-Gentil L, Cordonier A, et al. Environmental monitoring: inferring the diatom index from next-generation sequencing data. Environ Sci Technol. 2015;49(13):7597–7605.
   PubMed Web of Science ®Google Scholar