Unraveling Evolutionary Paths: Genomic Divergence and Geographic Secrets of Cylindrospermopsis and Sphaerospermopsis
Resumo
This study aims to investigate the biological diversity of 21 genomes of Cylindrospermopsis and 6 genomes of Sphaerospermopsis belonging to the family Aphanizomenonaceae using bioinformatics methods in comparative genomics. The comparative analysis of the lineages of the groups From the Americas, Non-Americas and Sphaerospermospsis revealed conserved central genome but with different accessory genomes by geographic region. The variations observed in the organization of saxitoxin and cylindrospermopsin genes in the accessory genome of Cylindrospermopsis raciborskii from the Americas and NonAmericas, suggests in the future the formation of a new taxonomic group, due to independent evolutionary trajectories.
Referências
Abreu, V. A. C., Popin, R. V., Alvarenga, D. O., Schaker, P. D. C., Hoff-Risseti, C., Varani, A. M., and Fiore, M. F. (2018). Genomic and Genotypic Characterization of Cylindrospermopsis raciborskii: Toward an Intraspecific Phylogenetic Evaluation by Comparative Genomics. Frontiers in Microbiology, 9. Publisher: Frontiers.
Antunes, J. T., Leão, P. N., and Vasconcelos, V. M. (2015). Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Frontiers in Microbiology, 6. Publisher: Frontiers.
Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., Meyer, F., Olsen, G. J., Olson, R., Osterman, A. L., Overbeek, R. A., McNeil, L. K., Paarmann, D., Paczian, T., Parrello, B., Pusch, G. D., Reich, C., Stevens, R., Vassieva, O., Vonstein, V., Wilke, A., and Zagnitko, O. (2008). The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics, 9(1):75.
Contreras-Moreira, B. and Vinuesa, P. (2013). GET_homologues, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis. Applied and Environmental Microbiology, 79(24):7696–7701. Publisher: American Society for Microbiology.
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and high-performance computing. Nature methods, 9(8):772.
Dreher, T. W., Davis, E. W., Mueller, R. S., and Otten, T. G. (2021). Comparative genomics of the ADA clade within the Nostocales. Harmful Algae, 104:102037.
Driscoll, C. B., Meyer, K. A., Šulčius, S., Brown, N. M., Dick, G. J., Cao, H., Gasiūnas, G., Timinskas, A., Yin, Y., Landry, Z. C., Otten, T. G., Davis, T. W., Watson, S. B., and Dreher, T. W. (2018). A closely-related clade of globally distributed bloom-forming cyanobacteria within the Nostocales. Harmful Algae, 77:93–107.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5):1792–1797.
Fuentes-Valdés, J. J., Soto-Liebe, K., Pérez-Pantoja, D., Tamames, J., Belmar, L., Pedrós-Alió, C., Garrido, D., and Vásquez, M. (2018). Draft genome sequences of Cylindrospermopsis raciborskii strains CS-508 and MVCC14, isolated from freshwater bloom events in Australia and Uruguay. Standards in Genomic Sciences, 13:26.
Hoff-Risseti, C., Dörr, F. A., Schaker, P. D. C., Pinto, E., Werner, V. R., and Fiore, M. F. (2013). Cylindrospermopsin and saxitoxin synthetase genes in Cylindrospermopsis raciborskii strains from Brazilian freshwater. PloS One, 8(8):e74238.
Hoffmann, L., Ramos, R. J. T., Guedes, I. A., Costa, P. F., Miguel, C. R. D., Azevedo, S. M. F. d. O. e., and Silva, R. (2017). Draft Genome Sequences of Two Brazilian Cyanobacterial Strains of Cylindrospermopsis raciborskii: Differences in Membrane Transporters, Saxitoxin Production, and Antioxidant Activities. Genome Announcements, 5(43). DOI: 10.1128/genomea.00879–17. Publisher: American Society for Microbiology.
Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M. H., and Visser, P. M. (2018). Cyanobacterial blooms. Nature Reviews Microbiology, 16(8):471–483. Publisher: Nature Publishing Group.
Kim, Y.-J., Park, H.-K., and Kim, I.-S. (2020). Invasion and toxin production by exotic nostocalean cyanobacteria (Cuspidothrix, Cylindrospermopsis, and Sphaerospermopsis) in the Nakdong River, Korea. Harmful Algae, 100:101954.
Klassen, J. L. and Currie, C. R. (2012). Gene fragmentation in bacterial draft genomes: extent, consequences and mitigation. BMC Genomics, 13(1):14.
Kokociński, M., Gągała, I., Jasser, I., Karosienė, J., Kasperovičienė, J., Kobos, J., Koreivienė, J., Soininen, J., Szczurowska, A., Woszczyk, M., and Mankiewicz-Boczek, J. (2017). Distribution of invasive Cylindrospermopsis raciborskii in the East-Central Europe is driven by climatic and local environmental variables. FEMS Microbiology Ecology, 93(4):fix035.
Kristensen, D. M., Kannan, L., Coleman, M. K., Wolf, Y. I., Sorokin, A., Koonin, E. V., and Mushegian, A. (2010). A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches. Bioinformatics, 26(12):1481–1487.
Laux, M., Piroupo, C. M., Setubal, J. C., and Giani, A. (2023). The Raphidiopsis (= Cylindrospermopsis) raciborskii pangenome updated: Two new metagenome-assembled genomes from the South American clade. Harmful Algae, 129:102518.
Li, L., Stoeckert, C. J., and Roos, D. S. (2003). OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes. Genome Research, 13(9):2178–2189. Company: Cold Spring Harbor Laboratory Press Distributor: Cold Spring Harbor Laboratory Press Institution: Cold Spring Harbor Laboratory Press Label: Cold Spring Harbor Laboratory Press Publisher: Cold Spring Harbor Lab.
Li, X., Yang, Y., Cai, F., Yang, P., Song, L., and Li, R. (2017). New insights into the taxonomy of the genus Sphaerospermopsis (Nostocales, Cyanobacteria) with the description of Sphaerospermopsis crassa sp. nov. Phycologia, 56(2):147–158. Publisher: Taylor & Francis.
Litchman, E. (2023). Understanding and predicting harmful algal blooms in a changing climate: A trait-based framework. Limnology and Oceanography Letters, 8(2):229–246. _eprint: [link].
Martins, J., Leikoski, N., Wahlsten, M., Azevedo, J., Antunes, J., Jokela, J., Sivonen, K., Vasconcelos, V., Fewer, D. P., and Leão, P. N. (2018). Sphaerocyclamide, a prenylated cyanobactin from the cyanobacterium Sphaerospermopsis sp. LEGE 00249. Scientific Reports, 8(1):14537. Publisher: Nature Publishing Group.
Medema, M. H., Blin, K., Cimermancic, P., de Jager, V., Zakrzewski, P., Fischbach, M. A., Weber, T., Takano, E., and Breitling, R. (2011). antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Research, 39(suppl_2):W339–W346.
Monteiro, P. R., do Amaral, S. C., Siqueira, A. S., Xavier, L. P., and Santos, A. V. (2021). Anabaenopeptins: What We Know So Far. Toxins, 13(8):522. Number: 8 Publisher: Multidisciplinary Digital Publishing Institute.
Nielsen, R. (2005). Statistical Methods in Molecular Evolution. Statistics for Biology and Health. Springer, New York, NY.
Padisák, J. (1997). Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. ARCHIV FÜR HYDROBIOLOGIE SUPPLEMENTBAND MONOGRAPHIS- CHE BEITRAGE, 107(4):563–593. Number: 4 Publisher: Schweizerbart.
Petkau, A., Stuart-Edwards, M., Stothard, P., and Van Domselaar, G. (2010). Interactive microbial genome visualization with GView. Bioinformatics, 26(24):3125–3126.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1):D590–D596. Accessed on:2022-08-19.
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4):406–425.
Sant’Anna, C. L., Gama, W. A., Rigonato, J., Correa, G., Mesquita, M. C. B., and Marinho, M. M. (2019). Phylogenetic connection among close genera of Aphanizomenonaceae (Cyanobacteria): Amphiheterocytum gen. nov., Cylindrospermopsis and Sphaerospermopsis. Algal Research, 37:205–214.
Scarlett, K. R., Kim, S., Lovin, L. M., Chatterjee, S., Scott, J. T., and Brooks, B. W. (2020). Global scanning of cylindrospermopsin: Critical review and analysis of aquatic occurrence, bioaccumulation, toxicity and health hazards. Science of The Total Environment, 738:139807.
Setubal, J. C., Almeida, N. F., and Wattam, A. R. (2018). Comparative Genomics for Prokaryotes. In Setubal, J. C., Stoye, J., and Stadler, P. F., editors, Comparative Genomics: Methods and Protocols, pages 55–78. Springer, New York, NY.
Sidelev, S., Koksharova, O., Babanazarova, O., Fastner, J., Chernova, E., and Gusev, E. (2020). Phylogeographic, toxicological and ecological evidence for the global distribution of Raphidiopsis raciborskii and its northernmost presence in Lake Nero, Central Western Russia. Harmful Algae, 98:101889.
Stampfli, G. M., Hochard, C., Vérard, C., Wilhem, C., and vonRaumer, J. (2013). The formation of Pangea. Tectonophysics, 593:1–19.
Tamura, K., Stecher, G., and Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7):3022–3027.
Teikari, J. E., Popin, R. V., Hou, S., Wahlsten, M., Hess, W. R., and Sivonen, K. (2019). Insight into the genome and brackish water adaptation strategies of toxic and bloom-forming Baltic Sea Dolichospermum sp. UHCC 0315. Scientific Reports, 9(1):4888. Publisher: Nature Publishing Group.
Vico, P., Bonilla, S., Cremella, B., Aubriot, L., Iriarte, A., and Piccini, C. (2020). Biogeography of the cyanobacterium Raphidiopsis (Cylindrospermopsis) raciborskii: Integrating genomics, phylogenetic and toxicity data. Molecular Phylogenetics and Evolution, 148:106824.
Voráčová, K., Hájek, J., Mareš, J., Urajová, P., Kuzma, M., Cheel, J., Villunger, A., Kapuscik, A., Bally, M., Novák, P., Kabeláč, M., Krumschnabel, G., Lukeš, M., Voloshko, L., Kopecký, J., and Hrouzek, P. (2017). The cyanobacterial metabolite nocuolin a is a natural oxadiazine that triggers apoptosis in human cancer cells. PLOS ONE, 12(3):e0172850. Publisher: Public Library of Science.
Wu, M. and Eisen, J. A. (2008). A simple, fast, and accurate method of phylogenomic inference. Genome Biology, 9(10):R151.
Zapomělová, E., Jezberová, J., Hrouzek, P., Hisem, D., Řeháková, K., and Komárková, J. (2009). Polyphasic Characterization of Three Strains of Anabaena Reniformis and Aphanizomenon Aphanizomenoides (cyanobacteria) and Their Reclassification to Sphaerospermum Gen. Nov. (incl. Anabaena Kisseleviana). Journal of Phycology, 45(6):1363–1373. _eprint: [link].
Antunes, J. T., Leão, P. N., and Vasconcelos, V. M. (2015). Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Frontiers in Microbiology, 6. Publisher: Frontiers.
Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., Meyer, F., Olsen, G. J., Olson, R., Osterman, A. L., Overbeek, R. A., McNeil, L. K., Paarmann, D., Paczian, T., Parrello, B., Pusch, G. D., Reich, C., Stevens, R., Vassieva, O., Vonstein, V., Wilke, A., and Zagnitko, O. (2008). The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics, 9(1):75.
Contreras-Moreira, B. and Vinuesa, P. (2013). GET_homologues, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis. Applied and Environmental Microbiology, 79(24):7696–7701. Publisher: American Society for Microbiology.
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and high-performance computing. Nature methods, 9(8):772.
Dreher, T. W., Davis, E. W., Mueller, R. S., and Otten, T. G. (2021). Comparative genomics of the ADA clade within the Nostocales. Harmful Algae, 104:102037.
Driscoll, C. B., Meyer, K. A., Šulčius, S., Brown, N. M., Dick, G. J., Cao, H., Gasiūnas, G., Timinskas, A., Yin, Y., Landry, Z. C., Otten, T. G., Davis, T. W., Watson, S. B., and Dreher, T. W. (2018). A closely-related clade of globally distributed bloom-forming cyanobacteria within the Nostocales. Harmful Algae, 77:93–107.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5):1792–1797.
Fuentes-Valdés, J. J., Soto-Liebe, K., Pérez-Pantoja, D., Tamames, J., Belmar, L., Pedrós-Alió, C., Garrido, D., and Vásquez, M. (2018). Draft genome sequences of Cylindrospermopsis raciborskii strains CS-508 and MVCC14, isolated from freshwater bloom events in Australia and Uruguay. Standards in Genomic Sciences, 13:26.
Hoff-Risseti, C., Dörr, F. A., Schaker, P. D. C., Pinto, E., Werner, V. R., and Fiore, M. F. (2013). Cylindrospermopsin and saxitoxin synthetase genes in Cylindrospermopsis raciborskii strains from Brazilian freshwater. PloS One, 8(8):e74238.
Hoffmann, L., Ramos, R. J. T., Guedes, I. A., Costa, P. F., Miguel, C. R. D., Azevedo, S. M. F. d. O. e., and Silva, R. (2017). Draft Genome Sequences of Two Brazilian Cyanobacterial Strains of Cylindrospermopsis raciborskii: Differences in Membrane Transporters, Saxitoxin Production, and Antioxidant Activities. Genome Announcements, 5(43). DOI: 10.1128/genomea.00879–17. Publisher: American Society for Microbiology.
Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M. H., and Visser, P. M. (2018). Cyanobacterial blooms. Nature Reviews Microbiology, 16(8):471–483. Publisher: Nature Publishing Group.
Kim, Y.-J., Park, H.-K., and Kim, I.-S. (2020). Invasion and toxin production by exotic nostocalean cyanobacteria (Cuspidothrix, Cylindrospermopsis, and Sphaerospermopsis) in the Nakdong River, Korea. Harmful Algae, 100:101954.
Klassen, J. L. and Currie, C. R. (2012). Gene fragmentation in bacterial draft genomes: extent, consequences and mitigation. BMC Genomics, 13(1):14.
Kokociński, M., Gągała, I., Jasser, I., Karosienė, J., Kasperovičienė, J., Kobos, J., Koreivienė, J., Soininen, J., Szczurowska, A., Woszczyk, M., and Mankiewicz-Boczek, J. (2017). Distribution of invasive Cylindrospermopsis raciborskii in the East-Central Europe is driven by climatic and local environmental variables. FEMS Microbiology Ecology, 93(4):fix035.
Kristensen, D. M., Kannan, L., Coleman, M. K., Wolf, Y. I., Sorokin, A., Koonin, E. V., and Mushegian, A. (2010). A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches. Bioinformatics, 26(12):1481–1487.
Laux, M., Piroupo, C. M., Setubal, J. C., and Giani, A. (2023). The Raphidiopsis (= Cylindrospermopsis) raciborskii pangenome updated: Two new metagenome-assembled genomes from the South American clade. Harmful Algae, 129:102518.
Li, L., Stoeckert, C. J., and Roos, D. S. (2003). OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes. Genome Research, 13(9):2178–2189. Company: Cold Spring Harbor Laboratory Press Distributor: Cold Spring Harbor Laboratory Press Institution: Cold Spring Harbor Laboratory Press Label: Cold Spring Harbor Laboratory Press Publisher: Cold Spring Harbor Lab.
Li, X., Yang, Y., Cai, F., Yang, P., Song, L., and Li, R. (2017). New insights into the taxonomy of the genus Sphaerospermopsis (Nostocales, Cyanobacteria) with the description of Sphaerospermopsis crassa sp. nov. Phycologia, 56(2):147–158. Publisher: Taylor & Francis.
Litchman, E. (2023). Understanding and predicting harmful algal blooms in a changing climate: A trait-based framework. Limnology and Oceanography Letters, 8(2):229–246. _eprint: [link].
Martins, J., Leikoski, N., Wahlsten, M., Azevedo, J., Antunes, J., Jokela, J., Sivonen, K., Vasconcelos, V., Fewer, D. P., and Leão, P. N. (2018). Sphaerocyclamide, a prenylated cyanobactin from the cyanobacterium Sphaerospermopsis sp. LEGE 00249. Scientific Reports, 8(1):14537. Publisher: Nature Publishing Group.
Medema, M. H., Blin, K., Cimermancic, P., de Jager, V., Zakrzewski, P., Fischbach, M. A., Weber, T., Takano, E., and Breitling, R. (2011). antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Research, 39(suppl_2):W339–W346.
Monteiro, P. R., do Amaral, S. C., Siqueira, A. S., Xavier, L. P., and Santos, A. V. (2021). Anabaenopeptins: What We Know So Far. Toxins, 13(8):522. Number: 8 Publisher: Multidisciplinary Digital Publishing Institute.
Nielsen, R. (2005). Statistical Methods in Molecular Evolution. Statistics for Biology and Health. Springer, New York, NY.
Padisák, J. (1997). Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. ARCHIV FÜR HYDROBIOLOGIE SUPPLEMENTBAND MONOGRAPHIS- CHE BEITRAGE, 107(4):563–593. Number: 4 Publisher: Schweizerbart.
Petkau, A., Stuart-Edwards, M., Stothard, P., and Van Domselaar, G. (2010). Interactive microbial genome visualization with GView. Bioinformatics, 26(24):3125–3126.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1):D590–D596. Accessed on:2022-08-19.
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4):406–425.
Sant’Anna, C. L., Gama, W. A., Rigonato, J., Correa, G., Mesquita, M. C. B., and Marinho, M. M. (2019). Phylogenetic connection among close genera of Aphanizomenonaceae (Cyanobacteria): Amphiheterocytum gen. nov., Cylindrospermopsis and Sphaerospermopsis. Algal Research, 37:205–214.
Scarlett, K. R., Kim, S., Lovin, L. M., Chatterjee, S., Scott, J. T., and Brooks, B. W. (2020). Global scanning of cylindrospermopsin: Critical review and analysis of aquatic occurrence, bioaccumulation, toxicity and health hazards. Science of The Total Environment, 738:139807.
Setubal, J. C., Almeida, N. F., and Wattam, A. R. (2018). Comparative Genomics for Prokaryotes. In Setubal, J. C., Stoye, J., and Stadler, P. F., editors, Comparative Genomics: Methods and Protocols, pages 55–78. Springer, New York, NY.
Sidelev, S., Koksharova, O., Babanazarova, O., Fastner, J., Chernova, E., and Gusev, E. (2020). Phylogeographic, toxicological and ecological evidence for the global distribution of Raphidiopsis raciborskii and its northernmost presence in Lake Nero, Central Western Russia. Harmful Algae, 98:101889.
Stampfli, G. M., Hochard, C., Vérard, C., Wilhem, C., and vonRaumer, J. (2013). The formation of Pangea. Tectonophysics, 593:1–19.
Tamura, K., Stecher, G., and Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7):3022–3027.
Teikari, J. E., Popin, R. V., Hou, S., Wahlsten, M., Hess, W. R., and Sivonen, K. (2019). Insight into the genome and brackish water adaptation strategies of toxic and bloom-forming Baltic Sea Dolichospermum sp. UHCC 0315. Scientific Reports, 9(1):4888. Publisher: Nature Publishing Group.
Vico, P., Bonilla, S., Cremella, B., Aubriot, L., Iriarte, A., and Piccini, C. (2020). Biogeography of the cyanobacterium Raphidiopsis (Cylindrospermopsis) raciborskii: Integrating genomics, phylogenetic and toxicity data. Molecular Phylogenetics and Evolution, 148:106824.
Voráčová, K., Hájek, J., Mareš, J., Urajová, P., Kuzma, M., Cheel, J., Villunger, A., Kapuscik, A., Bally, M., Novák, P., Kabeláč, M., Krumschnabel, G., Lukeš, M., Voloshko, L., Kopecký, J., and Hrouzek, P. (2017). The cyanobacterial metabolite nocuolin a is a natural oxadiazine that triggers apoptosis in human cancer cells. PLOS ONE, 12(3):e0172850. Publisher: Public Library of Science.
Wu, M. and Eisen, J. A. (2008). A simple, fast, and accurate method of phylogenomic inference. Genome Biology, 9(10):R151.
Zapomělová, E., Jezberová, J., Hrouzek, P., Hisem, D., Řeháková, K., and Komárková, J. (2009). Polyphasic Characterization of Three Strains of Anabaena Reniformis and Aphanizomenon Aphanizomenoides (cyanobacteria) and Their Reclassification to Sphaerospermum Gen. Nov. (incl. Anabaena Kisseleviana). Journal of Phycology, 45(6):1363–1373. _eprint: [link].
Publicado
02/12/2024
Como Citar
NOOBLATH, Reno S.; GOMES, Daniel H.; ALMEIDA, Sintia S.; ABREU, Vinícius A..
Unraveling Evolutionary Paths: Genomic Divergence and Geographic Secrets of Cylindrospermopsis and Sphaerospermopsis. In: SIMPÓSIO BRASILEIRO DE BIOINFORMÁTICA (BSB), 17. , 2024, Vitória/ES.
Anais [...].
Porto Alegre: Sociedade Brasileira de Computação,
2024
.
p. 179-190.
ISSN 2316-1248.
DOI: https://doi.org/10.5753/bsb.2024.245607.
