[en] An ongoing issue among cyanobacteriologists is the sometimes-mandatory obligation of working with axenic cultures. Proponents of axenicity argue that it is the safest way to determine the true producer of a particular compound, as a contaminant-free pure culture possesses only the targeted strain's genetic material. For biotechnological applications, axenicity allows the produced biomass to be used in valuable and high-end purposes, such as pharmaceutics, agriculture, cosmetic and food sectors. Nevertheless, axenic cultures are expensive and hard to obtain, requiring constant surveillance. Some strains are described as recalcitrant to axenicity, dying off or ceasing the biosynthesis of some compounds. Axenic culturing greatly deviates from natural conditions, which may alter gene expression and fail to embody ecological relationships. In non-axenic cultures, a complex interaction network among microorganisms exists, with shared metabolic pathways generating biochemical diversity that allows strains to survive stress and laboratory conditions. On the other hand, a non-axenic condition may limit the final use of the biomass produced, as unknown contaminants might be present. Additionally, depending on the ecological interaction established, competition between different microorganisms can negatively influence the growth of the targeted population. This review discusses axenicity in cyanobacterial research and the feasibility of performing high-quality scientific research without axenic cultures, presenting both culturing approaches and shedding light on the intricate nature of microbial interactions.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Dextro, Rafael B.; University of São Paulo (USP), Centre for Nuclear Energy in Agriculture (CENA), Piracicaba, Brazil
Andreote, Ana P.D.; University of São Paulo (USP), Centre for Nuclear Energy in Agriculture (CENA), Piracicaba, Brazil
Vaz, Marcelo ; Université de Liège - ULiège > Département des sciences de la vie > Centre d'Ingénierie des Protéines (CIP)
Carvalho, Carolinne R.; University of São Paulo (USP), Centre for Nuclear Energy in Agriculture (CENA), Piracicaba, Brazil ; College of Agriculture ‘Luiz de Queiroz’ (ESALQ), University of São Paulo, Piracicaba, Brazil
Fiore, Marli F.; University of São Paulo (USP), Centre for Nuclear Energy in Agriculture (CENA), Piracicaba, Brazil
Language :
English
Title :
The pros and cons of axenic cultures in cyanobacterial research
Publication date :
2024
Journal title :
Algal Research
ISSN :
2211-9264
Publisher :
Elsevier
Volume :
78
Pages :
103415
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior BELSPO - Belgian Federal Science Policy Office CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico FAPESP - Fundação de Amparo à Pesquisa do Estado de São Paulo
Funding text :
Grants from the State of São Paulo Research Foundation (FAPESP, 2016/14227-5 ) and Brazilian National Council for Scientific and Technological Development (CNPq, 433166/2018-5 ) supported this research. R.B.D. received funding from the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES, Finance Code 001 ) and a doctoral scholarship from CNPq (140892/2020-6). M.G.M.V.V. thanks the Belgian Science Policy Office that is supporting the BCCM/ULC collection. M.F.F. received a research fellowship (306803/2018-6) from CNPq.Grants from the State of São Paulo Research Foundation (FAPESP, 2016/14227-5) and Brazilian National Council for Scientific and Technological Development (CNPq, 433166/2018-5) supported this research. R.B.D. received funding from the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES, Finance Code 001) and a doctoral scholarship from CNPq (140892/2020-6). M.G.M.V.V. thanks the Belgian Science Policy Office that is supporting the BCCM/ULC collection. M.F.F. received a research fellowship (306803/2018-6) from CNPq.
Gao, S., Kong, Y., Yu, J., Miao, L., Ji, L., Song, L., Zeng, C., Isolation of axenic cyanobacterium and the promoting effect of associated bacterium on axenic cyanobacterium. BMC Biotechnol., 20, 2020, 61, 10.1186/s12896-020-00656-5.
Temraleeva, A.D., Dronova, S.A., Moskalenko, S.V., Didovich, S.V., Modern methods for isolation, purification, and cultivation of soil cyanobacteria. Microbiol. (Russian Fed.) 85 (2016), 389–399, 10.1134/S0026261716040159.
Rippka, R., Isolation and purification of cyanobacteria. Methods Enzymol, 1988, Academic Press, 3–27, 10.1016/0076-6879(88)67004-2.
Kearney, S.M., Coe, A., Castro, K.G., Chisholm, S.W., Filter plating method for rendering picocyanobacteria cultures free of heterotrophic bacterial contaminants and clonal. Front. Microbiol., 13, 2022, 10.3389/fmicb.2022.821803.
Wade, W., Unculturable bacteria - the uncharacterized organisms that cause oral infections. J. R. Soc. Med. 95 (2002), 81–83, 10.1258/jrsm.95.2.81.
Lewis, K., Epstein, S., D'Onofrio, A., Ling, L.L., Uncultured microorganisms as a source of secondary metabolites. J. Antibiot. (Tokyo) 63 (2010), 468–476, 10.1038/ja.2010.87.
Tanner, R.S., Cultivation of bacteria and fungi. Man. Environ. Microbiol, 2007, Wiley, 69–78, 10.1128/9781555815882.ch6.
Oren, A., Mareš, J., Rippka, R., Validation of the names cyanobacterium and cyanobacterium stanieri, and proposal of Cyanobacteriota phyl. nov. Int. J. Syst. Evol. Microbiol., 72, 2022, 10.1099/ijsem.0.005528.
Stanier, R.Y., Sistrom, W.R., Hansen, T.A., Proposal to place the nomenclature of the cyanbacteria (blue-green algae) under the rules of the international code of nomenclature of bacteria. Int. J. Syst. Bacteriol. 28 (1978), 335–336, 10.1099/00207713-28-2-335.
Waterbury, J.B., The cyanobacteria—isolation, purification and identification. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., Stackebrandt, E., (eds.) The Prokaryotes, 2006, Springer US, New York, NY, 1053–1073, 10.1007/0-387-30744-3_38.
Choi, C.W., Yoo, S.A., Oh, I.H., Park, S.H., Characterization of an extracellular flocculating substance produced by a planktonic cyanobacterium, Anabaena sp. Biotechnol. Lett. 20 (1998), 643–646, 10.1023/A:1005358204636.
Mohamed, Z.A., Allelopathic activity of the norharmane-producing cyanobacterium Synechocystis aquatilis against cyanobacteria and microalgae. Oceanol. Hydrobiol. Stud. 42 (2013), 1–7, 10.2478/s13545-013-0053-3.
Welker, M., Dittmann, E., Von Döhren, H., Cyanobacteria as a source of natural products. D.A.B.T.-M. in E. Hopwood, (eds.) Methods Enzymol, 2012, Academic Press, 23–46, 10.1016/B978-0-12-404634-4.00002-4.
Pringsheim, E.G., Zur physiologie der Schizophyceen. Beitr. Biol. Pflanzen. 12 (1914), 49–108.
Allen, M.B., The cultivation of myxophyceae. Arch. Mikrobiol. 17 (1952), 34–53, 10.1007/BF00410816.
van der Grinten, E., Pikkemaat, M.G., van den Brandhof, E.J., Stroomberg, G.J., Kraak, M.H.S., Comparing the sensitivity of algal, cyanobacterial and bacterial bioassays to different groups of antibiotics. Chemosphere 80 (2010), 1–6, 10.1016/j.chemosphere.2010.04.011.
Gantar, M., Sekar, R., Richardson, L.L., Cyanotoxins from black band disease of corals and from other coral reef environments. Microb. Ecol. 58 (2009), 856–864, 10.1007/s00248-009-9540-x.
Vaz, M.G.M.V., Bastos, R.W., Milanez, G.P., Moura, M.N., Ferreira, É.G., Perin, C., Pontes, M.C.F., do Nascimento, A.G., Use of sodium hypochlorite solutions to obtain axenic cultures of Nostoc strains (Cyanobacteria). Rev. Bras. Bot. 37 (2014), 115–120, 10.1007/s40415-014-0055-4.
Heck, K., Machineski, G.S., Alvarenga, D.O., Vaz, M.G.M.V., Varani, A. de M., Fiore, M.F., Evaluating methods for purifying cyanobacterial cultures by qPCR and high-throughput Illumina sequencing. J. Microbiol. Methods 129 (2016), 55–60, 10.1016/j.mimet.2016.07.023.
Vázquez-Martínez, G., Rodriguez, M.H., Hernández-Hernández, F., Ibarra, J.E., Strategy to obtain axenic cultures from field-collected samples of the cyanobacterium Phormidium animalis. J. Microbiol. Methods 57 (2004), 115–121, 10.1016/j.mimet.2003.12.003.
Ferris, M.J., Hirsch, C.F., Method for isolation and purification of cyanobacteria. Appl. Environ. Microbiol. 57 (1991), 1448–1452, 10.1128/aem.57.5.1448-1452.1991.
Sena, L., Rojas, D., Montiel, E., González, H., Moret, J., Naranjo, L., A strategy to obtain axenic cultures of Arthrospira spp. cyanobacteria. World J. Microbiol. Biotechnol. 27 (2011), 1045–1053, 10.1007/s11274-010-0549-6.
Cullen, J.J., MacIntyre, H.L., On the use of the serial dilution culture method to enumerate viable phytoplankton in natural communities of plankton subjected to ballast water treatment. J. Appl. Phycol. 28 (2016), 279–298, 10.1007/s10811-015-0601-x.
Franklin, R.B., Garland, J.L., Bolster, C.H., Mills, A.L., Impact of dilution on microbial community structure and functional potential: comparison of numerical simulations and batch culture experiments. Appl. Environ. Microbiol. 67 (2001), 702–712, 10.1128/AEM.67.2.702-712.2001.
Bowyer, J.W., Skerman, V.B., Production of axemic cultures of soil-borne and endophytic blue-green algae. J. Gen. Microbiol. 54 (1968), 299–306, 10.1099/00221287-54-2-299.
Vaara, T., Vaara, M., Niemela, S., Two improved methods for obtaining axenic cultures of cyanobacteria. Appl. Environ. Microbiol. 38 (1979), 1011–1014, 10.1128/aem.38.5.1011-1014.1979.
Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G., Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35 (1971), 171–205, 10.1128/br.35.2.171-205.1971.
Rippka, R., Waterbury, J.B., Stanier, R.Y., Isolation and purification of cyanobacteria: Some general principles. Starr, M.P., Stolp, H., Trüper, H.G., Balows, A., Schlegel, H.G., (eds.) The Prokaryotes, 1981, Springer Berlin Heidelberg, Berlin, Heidelberg, 212–220, 10.1007/978-3-662-13187-9_8.
Šulčius, S., Slavuckytė, K., Januškaitė, M., Paškauskas, R., Establishment of axenic cultures from cyanobacterium Aphanizomenon flos-aquae akinetes by micromanipulation and chemical treatment. Algal Res. 23 (2017), 43–50, 10.1016/j.algal.2017.01.006.
Wieringa, K.T., A new method for obtaining bacteria-free cultures of blue-green algae. Antonie Van Leeuwenhoek 34 (1968), 54–56, 10.1007/BF02046413.
Choi, G.G., Bae, M.S., Ahn, C.Y., Oh, H.M., Induction of axenic culture of Arthrospira (Spirulina) platensis based on antibiotic sensitivity of contaminating bacteria. Biotechnol. Lett. 30 (2008), 87–92, 10.1007/s10529-007-9523-2.
Kim, J.S., Park, Y.H., Yoon, B.D., Oh, H.M., Establishment of axenic cultures of Anabaena flos-aquae and Aphanothece nidulans (Cyanobacteria) by lysozyme treatment. J. Phycol. 35 (1999), 865–869, 10.1046/j.1529-8817.1999.3540865.x.
McDaniel, H.R., Middlebrook, J.B., Bowman, R.O., Isolation of pure cultures of algae from contaminated cultures. Appl. Microbiol., 10, 1962, 223, 10.1128/am.10.3.223-223.1962.
Carmichael, W.W., Gorham, P.R., An improved method for obtaining axenic clones of planktonic blue-green algae. J. Phycol. 10 (1974), 238–240, 10.1111/j.1529-8817.1974.tb02706.x.
Parker, D.L., Improved procedures for the cloning and purification of Microcystis cultures (Cyanophyta). J. Phycol. 18 (1982), 471–477, 10.1111/j.1529-8817.1982.tb03212.x.
de Siqueira Melo, R., Neves, M.H.C.B., Baptista, O.R., Axenic culture of the sea cyanobacterias Aphanothece halophytica Frémy, 1933 and Chroococcus minutus (Kützing) Nägeli, 1849. Acta Bot. Brasilica. 25 (2011), 234–240, 10.1590/S0102-33062011000100027.
Fogg, G.E., Studies on nitrogen fixation by blue-green algae. J. Exp. Biol. 19 (1942), 78–87, 10.1242/jeb.19.1.78.
Kaplan-Levy, R.N., Hadas, O., Summers, M.L., Rücker, J., Sukenik, A., Akinetes: dormant cells of cyanobacteria. Lubzens, E., Cerda, J., Clark, M., (eds.) Top. Curr. Genet, 2010, Springer Berlin Heidelberg, Berlin, Heidelberg, 5–27, 10.1007/978-3-642-12422-8_2.
R.W.B.T.-M. in E. Castenholz, [3] Culturing Methods for cyanobacteria. 1988, Cyanobacteria, Academic Press, 68–93, 10.1016/0076-6879(88)67006-6.
Azevedo, R., Rodriguez, E., Figueiredo, D., Peixoto, F., Santos, C., Methodologies for the study of filamentous cyanobacteria by flow cytometry. Fresen. Environ. Bull. 21 (2012), 679–684 http://surl.li/gqcnt.
Subashchandrabose, S.R., Ramakrishnan, B., Megharaj, M., Venkateswarlu, K., Naidu, R., Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol. Adv. 29 (2011), 896–907, 10.1016/j.biotechadv.2011.07.009.
Beliaev, A.S., Romine, M.F., Serres, M., Bernstein, H.C., Linggi, B.E., Markillie, L.M., Isern, N.G., Chrisler, W.B., Kucek, L.A., Hill, E.A., Pinchuk, G.E., Bryant, D.A., Steven Wiley, H., Fredrickson, J.K., Konopka, A., Inference of interactions in cyanobacterial-heterotrophic co-cultures via transcriptome sequencing. ISME J. 8 (2014), 2243–2255, 10.1038/ismej.2014.69.
Velmurugan, R., Incharoensakdi, A., Co-cultivation of two engineered strains of Synechocystis sp. PCC 6803 results in improved bioethanol production. Renew. Energy 146 (2020), 1124–1133, 10.1016/j.renene.2019.07.025.
Satpati, G.G., Pal, R., Co-cultivation of Leptolyngbya tenuis (Cyanobacteria) and Chlorella ellipsoidea (green alga) for biodiesel production, carbon sequestration, and cadmium accumulation. Curr. Microbiol. 78 (2021), 1466–1481, 10.1007/s00284-021-02426-8.
Das, P.K., Rani, J., Rawat, S., Kumar, S., Microalgal co-cultivation for biofuel production and bioremediation: current status and benefits. Bioenergy Res. 15 (2022), 1–26, 10.1007/s12155-021-10254-8.
González-Morales, S.I., Pacheco-Gutiérrez, N.B., Ramírez-Rodríguez, C.A., Brito-Bello, A.A., Estrella-Hernández, P., Herrera-Estrella, L., López-Arredondo, D.L., Metabolic engineering of phosphite metabolism in Synechococcus elongatus PCC 7942 as an effective measure to control biological contaminants in outdoor raceway ponds. Biotechnol. Biofuels, 13, 2020, 119, 10.1186/s13068-020-01759-z.
Wijffels, R.H., Kruse, O., Hellingwerf, K.J., Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr. Opin. Biotechnol. 24 (2013), 405–413, 10.1016/j.copbio.2013.04.004.
Buchan, A., LeCleir, G.R., Gulvik, C.A., González, J.M., Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Microbiol. 12 (2014), 686–698, 10.1038/nrmicro3326.
Seymour, J.R., Amin, S.A., Raina, J.B., Stocker, R., Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat. Microbiol., 2, 2017, 17065, 10.1038/nmicrobiol.2017.65.
Halary, S., Duperron, S., Demay, J., Duval, C., Hamlaoui, S., Piquet, B., Reinhardt, A., Bernard, C., Marie, B., Metagenome-based exploration of bacterial communities associated with cyanobacteria strains isolated from thermal muds. Microorganisms, 10, 2022, 2337, 10.3390/microorganisms10122337.
Pascault, N., Rué, O., Loux, V., Pédron, J., Martin, V., Tambosco, J., Bernard, C., Humbert, J.F., Leloup, J., Insights into the cyanosphere: capturing the respective metabolisms of cyanobacteria and chemotrophic bacteria in natural conditions?. Environ. Microbiol. Rep. 13 (2021), 364–374, 10.1111/1758-2229.12944.
Couradeau, E., Giraldo-Silva, A., De Martini, F., Garcia-Pichel, F., Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere. Microbiome 7 (2019), 1–12, 10.1186/s40168-019-0661-2.
Zhu, C.M., Zhang, J.Y., Guan, R., Hale, L., Chen, N., Li, M., Lu, Z.H., Ge, Q.Y., Yang, Y.F., Zhou, J.Z., Chen, T., Alternate succession of aggregate-forming cyanobacterial genera correlated with their attached bacteria by co-pathways. Sci. Total Environ. 688 (2019), 867–879, 10.1016/j.scitotenv.2019.06.150.
Baran, R., Brodie, E.L., Mayberry-Lewis, J., Hummel, E., Da Rocha, U.N., Chakraborty, R., Bowen, B.P., Karaoz, U., Cadillo-Quiroz, H., Garcia-Pichel, F., Northen, T.R., Exometabolite niche partitioning among sympatric soil bacteria. Nat. Commun., 6, 2015, 8289, 10.1038/ncomms9289.
Louati, I., Pascault, N., Debroas, D., Bernard, C., Humbert, J.F., Leloup, J., Structural diversity of bacterial communities associated with bloom-forming freshwater cyanobacteria differs according to the cyanobacterial genus. PloS One, 10, 2015, e0140614, 10.1371/journal.pone.0140614.
Xu, Z., Woodhouse, J.N., Te, S.H., Yew-Hoong Gin, K., He, Y., Xu, C., Chen, L., Seasonal variation in the bacterial community composition of a large estuarine reservoir and response to cyanobacterial proliferation. Chemosphere 202 (2018), 576–585, 10.1016/j.chemosphere.2018.03.037.
Berg, K.A., Lyra, C., Sivonen, K., Paulin, L., Suomalainen, S., Tuomi, P., Rapala, J., High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J. 3 (2009), 314–325, 10.1038/ismej.2008.110.
Zhang, Z., Tang, L., Liang, Y., Li, G., Li, H., Rivkin, R.B., Jiao, N., Zhang, Y., The relationship between two Synechococcus strains and heterotrophic bacterial communities and its associated carbon flow. J. Appl. Phycol. 33 (2021), 953–966, 10.1007/s10811-020-02343-6.
Grossart, H.P., Frindte, K., Dziallas, C., Eckert, W., Tang, K.W., Microbial methane production in oxygenated water column of an oligotrophic lake. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 19657–19661, 10.1073/pnas.1110716108.
Van Hannen, E.J., Zwart, G., Van Agterveld, M.P., Gons, H.J., Ebert, J., Laanbroek, H.J., Changes in bacterial and eukaryotic community structure after mass lysis of filamentous cyanobacteria associated with viruses. Appl. Environ. Microbiol. 65 (1999), 795–801, 10.1128/aem.65.2.795-801.1999.
Svercel, M., Saladin, B., Van Moorsel, S.J., Wolf, S., Bagheri, H.C., Antagonistic interactions between filamentous heterotrophs and the cyanobacterium Nostoc muscorum. BMC. Res. Notes, 4, 2011, 357, 10.1186/1756-0500-4-357.
Osman, O.A., Beier, S., Grabherr, M., Bertilsson, S., Interactions of freshwater cyanobacteria with bacterial antagonists. Appl. Environ. Microbiol., 83, 2017, 10.1128/AEM.02634-16.
Sukenik, A., Quesada, A., Salmaso, N., Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodivers. Conserv. 24 (2015), 889–908, 10.1007/s10531-015-0905-9.
Bizic, M., Phytoplankton photosynthesis: an unexplored source of biogenic methane emission from oxic environments. J. Plankton Res. 43 (2021), 822–830, 10.1093/plankt/fbab069.
Bruno, L., Billi, D., Albertano, P., Urzì, C., Genetic characterization of epilithic cyanobacteria and their associated bacteria. Geomicrobiol J. 23 (2006), 293–299, 10.1080/01490450600760732.
Van Wichelen, J., Vanormelingen, P., Codd, G.A., Vyverman, W., The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists. Harmful Algae 55 (2016), 97–111, 10.1016/j.hal.2016.02.009.
Jiang, L., Li, T., Jenkins, J., Hu, Y., Brueck, C.L., Pei, H., Betenbaugh, M.J., Evidence for a mutualistic relationship between the cyanobacteria Nostoc and fungi aspergilli in different environments. Appl. Microbiol. Biotechnol. 104 (2020), 6413–6426, 10.1007/s00253-020-10663-3.
Cooper, M.B., Smith, A.G., Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr. Opin. Plant Biol. 26 (2015), 147–153, 10.1016/j.pbi.2015.07.003.
Rosenberg, G., Paerl, H.W., Nitrogen fixation by blue-green algae associated with the siphonous green seaweed Codium decorticatum: effects on ammonium uptake. Mar. Biol. 61 (1981), 151–158, 10.1007/BF00386654.
Amin, S.A., Parker, M.S., Armbrust, E.V., Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76 (2012), 667–684, 10.1128/mmbr.00007-12.
Bauer, A., Forchhammer, K., Bacterial predation on cyanobacteria. Microb. Physiol. 31 (2021), 99–108, 10.1159/000516427.
Drakare, S., Competition between picoplanktonic cyanobacteria and heterotrophic bacteria along crossed gradients of glucose and phosphate. Microb. Ecol. 44 (2022), 327–335, 10.1007/s00248-002-1013-4.
Ji, X., Verspagen, J.M., Stomp, M., Huisman, J., Competition between cyanobacteria and green algae at low versus elevated CO2: who will win, and why?. J. Exp. Bot. 68 (2017), 3815–3828, 10.1093/jxb/erx027.
Roszak, D.B., Colwell, R.R., Survival strategies of bacteria in the natural environment. Microbiol. Rev. 51 (1987), 365–379, 10.1128/mr.51.3.365-379.1987.
Hugenholtz, P., Pace, N.R., Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. Trends Biotechnol. 14 (1996), 190–197, 10.1016/0167-7799(96)10025-1.
Wang, Z., Chen, Q., Zhang, J., Yan, H., Chen, Y., Chen, C., Chen, X., High prevalence of unstable antibiotic heteroresistance in cyanobacteria causes resistance underestimation. Water Res., 202, 2021, 117430, 10.1016/j.watres.2021.117430.
Amann, R.I., Ludwig, W., Schleifer, K.H., Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59 (1995), 143–169, 10.1128/mr.59.1.143-169.1995.
Schönhuber, W., Zarda, B., Eix, S., Rippka, R., Herdman, M., Ludwig, W., Amann, R., In situ identification of cyanobacteria with horseradish peroxidase- labeled, rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 65 (1999), 1259–1267, 10.1128/aem.65.3.1259-1267.1999.
Wang, X., Hu, M., Xia, Y., Wen, X., Ding, K., Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl. Environ. Microbiol. 78 (2012), 7042–7047, 10.1128/AEM.01617-12.
Props, R., Monsieurs, P., Mysara, M., Clement, L., Boon, N., Measuring the biodiversity of microbial communities by flow cytometry. Methods Ecol. Evol. 7 (2016), 1376–1385, 10.1111/2041-210X.12607.
Abreu, V.A.C., Popin, R.V., Alvarenga, D.O., Schaker, P.D.C., Hoff-Risseti, C., Varani, A.M., Fiore, M.F., Genomic and genotypic characterization of Cylindrospermopsis raciborskii: toward an intraspecific phylogenetic evaluation by comparative genomics. Front. Microbiol., 9, 2018, 10.3389/fmicb.2018.00306.
Rios, J.F., Leal, C.R., Leite, S.C., Janaina, R., Retz, C.L., Phenotypic plasticity and negative allelopathy in Microcystis strains. Ann. Microbiol. 66 (2016), 1265–1276, 10.1007/s13213-016-1215-5.
Pérez-Carrascal, O.M., Tromas, N., Terrat, Y., Moreno, E., Giani, A., Marques, L. Corrêa Braga, Fortin, N., Shapiro, B.J., Single-colony sequencing reveals microbe-by-microbiome phylosymbiosis between the cyanobacterium Microcystis and its associated bacteria. Microbiome 9 (2021), 1–21, 10.1186/s40168-021-01140-8.
Dextro, R.B., Delbaje, E., Geraldes, V., Pinto, E., Long, P.F., Fiore, M.F., Exploring the relationship between biosynthetic gene clusters and constitutive production of Mycosporine-like amino acids in Brazilian cyanobacteria. Molecules, 28, 2023, 1420, 10.3390/molecules28031420.
Magdouli, S., Brar, S.K., Blais, J.F., Co-culture for lipid production: advances and challenges. Biomass Bioenergy 92 (2016), 20–30, 10.1016/j.biombioe.2016.06.003.
Dextro, R.B., Growth dynamic on a co-cultivation of two chlorophyta microalgae exposed to copper. Acta Limnol. Bras., 33, 2021, 10.1590/S2179-975X0420.
Mlouka, A., Comte, K., Castets, A.M., Bouchier, C., Tandeau De Marsac, N., The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy. J. Bacteriol. 186 (2004), 2355–2365, 10.1128/JB.186.8.2355-2365.2004.
Meixner, K., Daffert, C., Bauer, L., Drosg, B., Fritz, I., PHB producing cyanobacteria found in the neighborhood— their isolation, purification and performance testing. Bioengineering, 9, 2022, 178, 10.3390/bioengineering9040178.
Soares, M.C.S., Lürling, M., Huszar, V.L.M., Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Phycol. Res. 61 (2013), 61–67, 10.1111/pre.12001.
Xiao, M., Li, M., Reynolds, C.S., Colony formation in the cyanobacterium Microcystis. Biol. Rev. 93 (2018), 1399–1420, 10.1111/brv.12401.
Dunker, S., Jakob, T., Wilhelm, C., Contrasting effects of the cyanobacterium Microcystis aeruginosa on the growth and physiology of two green algae, Oocystis marsonii and Scenedesmus obliquus, revealed by flow cytometry. Freshw. Biol. 58 (2013), 1573–1587, 10.1111/fwb.12143.
Lee, Y.K., Commercial production of mciroalgae in the Asia-Pacific rim. J. Appl. Phycol. 9 (1997), 403–411, 10.1023/A:1007900423275.
Spolaore, P., Joannis-Cassan, C., Duran, E., Isambert, A., Commercial applications of microalgae. J. Biosci. Bioeng. 101 (2006), 87–96, 10.1263/jbb.101.87.
Nwoba, E.G., Parlevliet, D.A., Laird, D.W., Alameh, K., Moheimani, N.R., Sustainable phycocyanin production from Arthrospira platensis using solar-control thin film coated photobioreactor. Biochem. Eng. J. 141 (2019), 232–238, 10.1016/j.bej.2018.10.024.
Eriksen, N.T., Production of phycocyanin - a pigment with applications in biology, biotechnology, foods and medicine. Appl. Microbiol. Biotechnol. 80 (2008), 1–14, 10.1007/s00253-008-1542-y.
Chaillan, F., Gugger, M., Saliot, A., Couté, A., Oudot, J., Role of cyanobacteria in the biodegradation of crude oil by a tropical cyanobacterial mat. Chemosphere 62 (2006), 1574–1582, 10.1016/j.chemosphere.2005.06.050.
Abed, R.M.M., Köster, J., The direct role of aerobic heterotrophic bacteria associated with cyanobacteria in the degradation of oil compounds. Int. Biodeterior. Biodegrad. 55 (2005), 29–37, 10.1016/j.ibiod.2004.07.001.
Abed, R.M.M., Interaction between cyanobacteria and aerobic heterotrophic bacteria in the degradation of hydrocarbons. Int. Biodeterior. Biodegrad. 64 (2010), 58–64, 10.1016/j.ibiod.2009.10.008.
Merel, S., Walker, D., Chicana, R., Snyder, S., Baurès, E., Thomas, O., State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ. Int. 59 (2013), 303–327, 10.1016/j.envint.2013.06.013.
Castro, D., Vera, D., Lagos, N., García, C., Vásquez, M., The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon 44 (2004), 483–489, 10.1016/j.toxicon.2004.06.005.
Sant'Anna, C.L., De Carvalho, L.R., Fiore, M.F., Silva-Stenico, M.E., Lorenzi, A.S., Rios, F.R., Konno, K., Garcia, C., Lagos, N., Highly toxic Microcystis aeruginosa strain, isolated from São Paulo-Brazil, produce hepatotoxins and paralytic shellfish poison neurotoxins. Neurotox. Res. 19 (2011), 389–402, 10.1007/s12640-010-9177-z.
Bates, S.S., Douglas, D.J., Doucette, G.J., Léger, C., Enhancement of domoic acid production by reintroducing bacteria to axenic cultures of the diatom Pseudo-nitzschia multiseries. Nat. Toxins 3 (1995), 428–435, 10.1002/nt.2620030605.
Hamlaoui, S., Yéprémian, C., Duval, C., Marie, B., Djédiat, C., Piquet, B., Bernard, C., Duperron, S., The culture collection of cyanobacteria and microalgae at the French National Museum of Natural History: a century old but still alive and kicking! Including in memoriam: professor Alain Couté. Cryptogam. Algol. 43 (2022), 41–83, 10.5252/cryptogamie-algologie2022v43a3.
Anam, M., Yousaf, S., Sharafat, I., Zafar, Z., Ayaz, K., Ali, N., Comparing natural and artificially designed bacterial consortia as biosensing elements for rapid non- specific detection of organic pollutant through microbial fuel cell. Int. J. Electrochem. Sci. 12 (2017), 2836–2851, 10.20964/2017.04.49.
Halfhide, T., Åkerstrøm, A., Lekang, O.I., Gislerød, H.R., Ergas, S.J., Production of algal biomass, chlorophyll, starch and lipids using aquaculture wastewater under axenic and non-axenic conditions. Algal Res. 6 (2014), 152–159, 10.1016/j.algal.2014.10.009.
Bidyarani, N., Prasanna, R., Chawla, G., Babu, S., Singh, R., Deciphering the factors associated with the colonization of rice plants by cyanobacteria. J. Basic Microbiol. 55 (2015), 407–419, 10.1002/jobm.201400591.
Bahareh Nowruzi, N., Bouaïcha, J.S., Metcalf, S.J., Porzani, O. Konur, Plant-cyanobacteria interactions: beneficial and harmful effects of cyanobacterial bioactive compounds on soil-plant systems and subsequent risk to animal and human health. Phytochemistry, 192, 2021, 112959, 10.1016/j.phytochem.2021.112959.
Rana, A., Joshi, M., Prasanna, R., Shivay, Y.S., Nain, L., Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur. J. Soil Biol. 50 (2012), 118–126, 10.1016/j.ejsobi.2012.01.005.
Singh, S., A review on possible elicitor molecules of cyanobacteria: their role in improving plant growth and providing tolerance against biotic or abiotic stress. J. Appl. Microbiol. 117 (2014), 1221–1244, 10.1111/jam.12612.
Hussain, A., Hasnain, S., Phytostimulation and biofertilization in wheat by cyanobacteria. J. Ind. Microbiol. Biotechnol. 38 (2011), 85–92, 10.1007/s10295-010-0833-3.
Nowruzi, B., Hutárová, L., Absalón, I.B., Liu, L., A new strain of Neowestiellopsis (Hapalosiphonaceae): first observation of toxic soil cyanobacteria from agricultural fields in Iran. BMC Microbiol., 22, 2022, 107, 10.1186/s12866-022-02525-x.
Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M., Tabata, S., Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3 (1996), 109–136, 10.1093/dnares/3.3.109.
Design of microbial consortia for industrial biotechnology. Höffner, K., Barton, P.I., Eden, M.R., Siirola, J.D., Towler, G.P.B.T.-C.A.C.E., (eds.) Comput. Aided Chem. Eng, 2014, Elsevier, 65–74, 10.1016/B978-0-444-63433-7.50008-0.
Tang, X., He, L.Y., Tao, X.Q., Dang, Z., Guo, C.L., Lu, G.N., Yi, X.Y., Construction of an artificial microalgal-bacterial consortium that efficiently degrades crude oil. J. Hazard. Mater. 181 (2010), 1158–1162, 10.1016/j.jhazmat.2010.05.033.
Pinevich, A.V., Andronov, E.E., Pershina, E.V., Pinevich, A.A., Dmitrieva, H.Y., Testing culture purity in prokaryotes: criteria and challenges, Antonie van Leeuwenhoek. Int. J. Gen. Mol. Microbiol. 111 (2018), 1509–1521, 10.1007/s10482-018-1054-4.
Hedlund, B.P., Chuvochina, M., Hugenholtz, P., Konstantinidis, K.T., Murray, A.E., Palmer, M., Parks, D.H., Probst, A.J., Reysenbach, A.L., Rodriguez-R, L.M., Rossello-Mora, R., Sutcliffe, I.C., Venter, S.N., Whitman, W.B., SeqCode: a nomenclatural code for prokaryotes described from sequence data. Nat. Microbiol. 7 (2022), 1702–1708, 10.1038/s41564-022-01214-9.
Alvarenga, D.O., Fiore, M.F., Varani, A.M., A metagenomic approach to cyanobacterial genomics. Front. Microbiol., 8, 2017, 10.3389/fmicb.2017.00809.
Lee, I., Chalita, M., Ha, S.M., Na, S.I., Yoon, S.H., Chun, J., ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int. J. Syst. Evol. Microbiol. 67 (2017), 2053–2057, 10.1099/ijsem.0.001872.
Parks, D.H., Imelfort, M., Skennerton, C.T., Hugenholtz, P., Tyson, G.W., CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25 (2015), 1043–1055, 10.1101/gr.186072.114.
Wirth, R., Pap, B., Böjti, T., Shetty, P., Lakatos, G., Bagi, Z., Kovács, K.L., Maróti, G., Chlorella vulgaris and its phycosphere in wastewater: microalgae-bacteria interactions during nutrient removal. Front. Bioeng. Biotechnol., 8, 2020, 10.3389/fbioe.2020.557572.
Cornet, L., Bertrand, A.R., Hanikenne, M., Javaux, E.J., Wilmotte, A., Baurain, D., Metagenomic assembly of new (sub)polar cyanobacteria and their associated microbiome from non-axenic cultures. Microb. Genomics., 4, 2018, 10.1099/mgen.0.000212.
Zhu, L., Zuo, J., Song, L., Gan, N., Microcystin-degrading bacteria affect mcyD expression and microcystin synthesis in Microcystis spp. J. Environ. Sci. (China) 41 (2016), 195–201, 10.1016/j.jes.2015.06.016.
Marcy, Y., Ouverney, C., Bik, E.M., Lösekann, T., Ivanova, N., Martin, H.G., Szeto, E., Platt, D., Hugenholtz, P., Relman, D.A., Quake, S.R., Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 11889–11894, 10.1073/pnas.0704662104.
Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N.N., Anderson, I.J., Cheng, J.F., Darling, A., Malfatti, S., Swan, B.K., Gies, E.A., Dodsworth, J.A., Hedlund, B.P., Tsiamis, G., Sievert, S.M., Liu, W.T., Eisen, J.A., Hallam, S.J., Kyrpides, N.C., Stepanauskas, R., Rubin, E.M., Hugenholtz, P., Woyke, T., Insights into the phylogeny and coding potential of microbial dark matter. Nature 499 (2013), 431–437, 10.1038/nature12352.
Dextro, R.B., Delbaje, E., Cotta, S.R., Zehr, J.P., Fiore, M.F., Trends in free-access genomic data accelerate advances in cyanobacteria taxonomy. J. Phycol. 57 (2021), 1392–1402, 10.1111/jpy.13200.
Imachi, H., Nobu, M.K., Miyazaki, M., Tasumi, E., Saito, Y., Sakai, S., Ogawara, M., Ohashi, A., Takai, K., Cultivation of previously uncultured microorganisms with a continuous-flow down-flow hanging sponge (DHS) bioreactor, using a syntrophic archaeon culture obtained from deep marine sediment as a case study. Nat. Protoc. 17 (2022), 2784–2814, 10.1038/s41596-022-00735-1.
Parks, D.H., Rinke, C., Chuvochina, M., Chaumeil, P.A., Woodcroft, B.J., Evans, P.N., Hugenholtz, P., Tyson, G.W., Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2 (2017), 1533–1542, 10.1038/s41564-017-0012-7.
Liu, S., Moon, C.D., Zheng, N., Huws, S., Zhao, S., Wang, J., Opportunities and challenges of using metagenomic data to bring uncultured microbes into cultivation. Microbiome, 10, 2022, 76, 10.1186/s40168-022-01272-5.
