Abstract
Microalgae are versatile sources of bioproducts, a solution for many environmental problems. However, and despite its importance, one of the main problems in large-scale cultures—the presence of contaminants—is rarely systematically approached. Contamination, or the presence of undesirable organisms in a culture, is deleterious for the culture and frequently leads to culture crashes. To avoid contamination, closed systems can be used; however, for very large-scale open systems, contamination is unavoidable and remediation procedures are necessary—ranging from physicochemical treatment to addition of biocidal substances. In all cases, early detection and culture monitoring are paramount. This article describes the biological contaminants, contamination mechanisms, and control systems used in open and closed cultures, discussing the latest advances and techniques in the area. It also discusses the complex interactions of algae with other microorganisms that can be expected in cultivation systems.
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References
Abeliovich A, Dikbuck S (1977) Factors Affecting Infection of Scenedesmus obliquus by a Chytridium sp. in Sewage Oxidation Ponds. Appl Environ Microbiol 34:832–836
Abeliovich A, Arad S, Becker W, Ben-Amotz A, Benemann JR, Yonghong B, Blackburn S, Boussiba S, Cysewski G, Fernandez AF, Grima EM, Grobbelaar JU, Danxiang H, Harel M, Zhengyu H, Iwamoto H, Jones IS, Kaplan D, Koblizek M, Lorenz T, Masojidek J, Redina A R, Muller-Feuga A, Place AR, Hu Q (2005) Handbook of microalgal culture. 577. https://doi.org/10.1002/9780470995280
Abou-waly H, Nigg HN, Mallory LL (1991) Growth response of freshwater algae, Anabaena flos-aquae and Selenastrum capricornutum to atrazine and hexazinone herbicides. Bull Environ Contam Toxicol 46:223–229
Ahmad M, Saleem MA, Sayyed AH (2009) Efficacy of insecticide mixtures against pyrethroid- and organophosphate-resistant populations of Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci 65:266–274. https://doi.org/10.1002/ps.1681
Amaral R, Pereira JC, Pais AACC, Santos LMA (2013) Is axenicity crucial to cryopreserve microalgae? Cryobiology 67:312–320. https://doi.org/10.1016/j.cryobiol.2013.09.006
Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101. https://doi.org/10.1038/nature14488
Anderson RA (2005) Algal culturing techniques, 1st edn
Angelis S, Novak AC, Sydney EB, Soccol VT, Carvalho JC, Pandey A, Noseda MD, Tholozan JL, Lorquin J, Soccol CR (2012) Co-culture of microalgae, cyanobacteria, and macromycetes for exopolysaccharides production: process preliminary optimization and partial characterization. Appl Biochem Biotechnol 167:1092–1106. https://doi.org/10.1007/s12010-012-9642-7
Aráoz R, Nghiêm HO, Rippka R, Palibroda N, Tandeau de Marsac N, Herdman M (2005) Neurotoxins in axenic oscillatorian cyanobacteria: coexistence of anatoxin-a and homoanatoxin-a determined by ligand-binding assay and GC/MS. Microbiology 151:1263–1273. https://doi.org/10.1099/mic.0.27660-0
Azov Y, Goldman JC (1982) Free ammonia inhibition of algal photosynthesis in intensive cultures. Appl Environ Microbiol 43:735–739
Bajpai VK, Kang S, Xu H, Lee SG, Baek KH, Kang SC (2011) Potential roles of essential oils on controlling plant pathogenic bacteria Xanthomonas species: a review. Plant Pathol J 27:207–224. https://doi.org/10.5423/PPJ.2011.27.3.207
Benson (2001) Microbiological applications lab manual. The McGraw-Hill Companies, 8th Ed
Berney C, Romac S, Mahé F, Santini S, Siano R, Bass D (2013) Vampires in the oceans: predatory cercozoan amoebae in marine habitats. ISME J 7:1–13. https://doi.org/10.1038/ismej.2013.116
Bogen C, Klassen V, Wichmann J, La Russa M, Doebbe A, Grundmann M, Uronen P, Kruse O, Mussgnug JH (2013) Identification of Monoraphidium contortum as a promising species for liquid biofuel production. Bioresour Technol 133:622–626. https://doi.org/10.1016/j.biortech.2013.01.164
Carney LT, Lane A (2015) Parasites in algae mass culture. In: Sime-Ngando T, Lafferty KD, Biron DG (eds) Roles and Mechanisms of parasitism in aquatic microbial communities, p 155
Cea-Barcia G, Buitrón G, Moreno G, Kumar G (2014) A cost-effective strategy for the bio-prospecting of mixed microalgae with high carbohydrate content: diversity fluctuations in different growth media. Bioresour Technol 163:370–373. https://doi.org/10.1016/j.biortech.2014.04.079
Centella MH, Arévalo-Gallego A, Parra-Saldivar R, Iqbal HMN (2017) Marine-derived bioactive compounds for value-added applications in bio- and non-bio sectors. J Clean Prod 168:1559–1565. https://doi.org/10.1016/j.jclepro.2017.05.086
Cho DH, Ramanan R, Kim BH, Lee J, Kim S, Yoo C, Choi GG, Oh HM, Kim HS (2013) Novel approach for the development of axenic microalgal cultures from environmental samples. J Phycol 49:802–810. https://doi.org/10.1111/jpy.12091
Cho DH, Ramanan R, Heo J, Lee J, Kim BH, Oh HM, Kim HS (2015) Enhancing microalgal biomass productivity by engineering a microalgal-bacterial community. Bioresour Technol 175:578–585. https://doi.org/10.1016/j.biortech.2014.10.159
Choi GG, Bae MS, Ahn CY, Oh HM (2008) Induction of axenic culture of Arthrospira (Spirulina) platensis based on antibiotic sensitivity of contaminating bacteria. Biotechnol Lett 30:87–92. https://doi.org/10.1007/s10529-007-9523-2
Cole J (1994) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13 (1):291–314
Croft MT, Lawrence AD, Raux-deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B 12 through a symbiotic relationship with bacteria. Nature 438:90–93. https://doi.org/10.1038/nature04056
Davies J, Davies D (2010) Origins and Evolution of Antibiotic Resistance. Microbiol Mol Biol Rev 74:417–433. https://doi.org/10.1128/MMBR.00016-10
Day JG, Thomas NJ, Achilles-Day UEM, Leakey RJG (2012) Early detection of protozoan grazers in algal biofuel cultures. Bioresour Technol 114:715–719. https://doi.org/10.1016/j.biortech.2012.03.015
Day JG, Gong Y, Hu Q (2017) Microzooplanktonic grazers—a potentially devastating threat to the commercial success of microalgal mass culture. Algal Res 27:356–365. https://doi.org/10.1016/j.algal.2017.08.024
de Araujo AB, Snell TW, Hagiwara A (2000) Effect of unionized ammonia, viscozity and protozoan contamination on the enzyme activity of the rotifer Brachionus plicalitis. Aquac Res 31:359–365
de-Bashan LE, Bashan Y, Moreno M, Lebsky VK, Bustillos JJ (2002) Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. Can J Microbiol 48:514–521. https://doi.org/10.1139/W02-051
Dryden RC, Wright SJL (1984) Predation of cyanobacteria by protoza. J Protozool 31:A42–A43
Fischer BB, Roffler S, Eggen RIL (2012) Multiple stressor effects of predation by rotifers and herbicide pollution on different Chlamydomonas strains and potential impacts on population dynamics. Environ Toxicol Chem 31:2832–2840. https://doi.org/10.1002/etc.2010
Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50. https://doi.org/10.1038/nrmicro2242
Forehead HI, O’Kelly CJ (2013) Small doses, big troubles: modeling growth dynamics of organisms affecting microalgal production cultures in closed photobioreactors. Bioresour Technol 129:329–334. https://doi.org/10.1016/j.biortech.2012.11.082
Frederiksen M, Edwards M, Richardson AJ, Halliday NC, Wanless S (2006) From plankton to top predators: bottom-up control of a marine food web across four trophic levels. J Anim Ecol 75:1259–1268. https://doi.org/10.1111/j.1365-2656.2006.01148.x
Fulbright SP, Dean MK, Wardle G, Lammers PJ, Chisholm S (2014) Molecular diagnostics for monitoring contaminants in algal cultivation. Algal Res 4:41–51. https://doi.org/10.1016/j.algal.2013.11.008
Gachon CMM, Strittmatter M, Müller DG, Kleinteich J, Küpper FC (2009) Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal. Appl Environ Microbiol 75:322–328. https://doi.org/10.1128/AEM.01885-08
Gerphagnon M, Latour D, Colombet J, Sime-Ngando T (2013) Fungal parasitism: life cycle, dynamics and impact on cyanobacterial blooms. PLoS One 8:2–11. https://doi.org/10.1371/journal.pone.0060894
Goers L, Freemont P, Polizzi KM (2014) Co-culture systems and technologies: taking synthetic biology to the next level. J R Soc Interface 11:20140065. https://doi.org/10.1098/rsif.2014.0065
Gomez-Gil B, Thompson F, Thompson C, Garcia-Gasca A, Roque A, Swings J (2004) Errata Vibrio hispanicus sp. nov., isolated from Artemia sp. and sea water in Spain. Int J Syst Evol Microbiol 54:63177–63177. https://doi.org/10.1099/ijs.0.63177-0
Gong Y, Patterson DJ, Li Y, Hu Z, Sommerfeld M, Chen Y, Hu Q (2015) Vernalophrys algivore gen. nov., sp. nov. (Rhizaria: Cercozoa: Vampyrellida), a new algal predator isolated from outdoor mass culture of Scenedesmus dimorphus. Appl Environ Microbiol 81:3900–3913. https://doi.org/10.1128/AEM.00160-15
Gonzalez LUZ, Bashan Y (2000) Increased Growth of the Microalga Chlorella vulgaris when Coimmobilized and Cocultured in Alginate Beads with the Plant-Growth-Promoting Bacterium Azospirillum brasilense. Appl Environ Microbiol 66:1527–1531
Gonzalez-Lopez CV, Ceron-Garcia MC, Fernandez-Sevilla JM, Gonzalezlez-Cesspedes AM, Camacho-Rodriguez J, Molina-Grima E (2013) Medium recycling for Nannochloropsis gaditana cultures for aquaculture. Bioresour Technol 129:430–438. https://doi.org/10.1016/j.biortech.2012.11.061
Grahl T, Märkl H (1996) Killing of micro-organisms by pulsed electric fields. Appl Microbiol Biotechnol 45:148–157
Grover JP (2000) Resource competition and community structure in aquatic micro-organisms: experimental studies of algae and bacteria along a gradient of organic carbon to inorganic phosphorus supply. J Plankton Res 22:1591–1610. https://doi.org/10.1093/plankt/22.8.1591
Guerrini F, Mazzotti A, Boni L, Pistocchi R (1998) Bacterial-algal interaction in polysaccharide production. Aquat Microb Ecol 15:247–253. https://doi.org/10.3354/ame015247
Guillard RRL (2005) Purification methods for microalgae. In: Algal culturing techniques. Elsevier Academic Press USA, Cambridge, pp 117–132
Guo Z, Tong YW (2014) The interactions between Chlorella vulgaris and algal symbiotic bacteria under photoautotrophic and photoheterotrophic conditions. J Appl Phycol 26:1483–1492. https://doi.org/10.1007/s10811-013-0186-1
Gutterman Y (1994) Algal allelopathy. Bot Rev 60:373–425
Hagiwara A, Gallardo WG, Assavaaree M, Kotani T, De Araujo AB (2001) Live food production in Japan: recent progress and future aspects. Aquaculture 200:111–127. https://doi.org/10.1016/S0044-8486(01)00696-2
Han J, Wang S, Zhang L, Yang G, Zhao L, Pan K (2016) A method of batch-purifying microalgae with multiple antibiotics at extremely high concentrations. Chin J Oceanol Limnol 34:79–85. https://doi.org/10.1007/s00343-015-4288-2
Haraguchi L, Jakobsen HH, Lundholm N, Carstensen J (2018) Phytoplankton community dynamic: a driver for ciliate trophic strategies. Front Mar Sci 5:1–16. https://doi.org/10.3389/fmars.2018.00272
Harrison DEF (1978) Mixed cultures in industrial fermentation processes. Adv Appl Microbiol 24:129–164. https://doi.org/10.1016/S0065-2164(08)70638-5
Hernández JP, De-Bashan LE, Bashan Y (2006) Starvation enhances phosphorus removal from wastewater by the microalga Chlorella spp. co-immobilized with Azospirillum brasilense. Enzyme Microb Technol 38:190–198. https://doi.org/10.1016/j.enzmictec.2005.06.005
Hess S, Sausen N, Melkonian M (2012) Shedding light on vampires: the phylogeny of vampyrellid amoebae revisited. PLoS One 7:e31165. https://doi.org/10.1371/journal.pone.0031165
Hesseltine CW et al (1992) Mixed-culture fermentations. In: Application of biotechnology for traditional fermented foods. National Academy Press, Washington D.C., pp 52–58
Hidalgo D, Mussons ML, Martín-Marroquín JM, Corona F (2018) Combined remediation and protein production using microalgae growth on waste bakery products. Waste Biomass Valor 9:2413–2422. https://doi.org/10.1007/s12649-018-0216-y
Hoffman Y, Aflalo C, Zarka A, Gutman J, James TY, Boussiba S (2008) Isolation and characterization of a novel chytrid species (phylum Blastocladiomycota), parasitic on the green alga Haematococcus. Mycol Res 112:70–81. https://doi.org/10.1016/j.mycres.2007.09.002
Huang Y, Li L, Liu J, Lin W (2014a) Botanical pesticides as potential rotifer-control agents in microalgal mass culture. Algal Res 4:62–69. https://doi.org/10.1016/j.algal.2013.08.001
Huang Y, Liu J, Li L, Pang T, Zhang L (2014b) Efficacy of binary combinations of botanical pesticides for rotifer elimination in microalgal cultivation. Bioresour Technol 154:67–73. https://doi.org/10.1016/j.biortech.2013.11.098
Huang Y, Liu J, Wang H, Gao Z (2014c) Treatment potential of a synergistic botanical pesticide combination for rotifer extermination during outdoor mass cultivation of Spirulina platensis. Algal Res 6:139–144. https://doi.org/10.1016/j.algal.2014.11.003
Ide K, Takahashi K, Kuwata A, Nakamachi M, Saito H (2008) A rapid analysis of copepod feeding using FlowCAM. J Plankton Res 30:275–281. https://doi.org/10.1093/plankt/fbm108
Imai I, Sunahara T, Nishikawa T, Hori Y, Kondo R, Hiroishi S (2001) Fluctuations of the red tide flagellates Chattonella spp. (Raphidophyceae) and the algicidal bacterium Cytophaga sp. in the Seto Inland Sea, Japan. Mar Biol 138:1043–1049. https://doi.org/10.1007/s002270000513
Kalia AMR (2011) Bioaugmentation, biostimulation and biocontrol. In: Ajay S, Kuhad NPRC (eds) Bioaugmentation, bioestimulation and biocontrol. Springer, Berlin, pp 223–240
Kan Y, Pan J (2010) A one-shot solution to bacterial and fungal contamination in the green alga Chlamydomonas Reinhardtii culture by using an antibiotic cocktail. J Phycol 46:1356–1358. https://doi.org/10.1111/j.1529-8817.2010.00904.x
Kong J, Xie YF, Guo YH, Cheng YL, Qian H, Yao WR (2016) Biocontrol of postharvest fungal decay of tomatoes with a combination of thymol and salicylic acid screening from 11 natural agents. LWT Food Sci Technol 72:215–222. https://doi.org/10.1016/j.lwt.2016.04.020
Krohn-Molt I, Wemheuer B, Alawi M, Poehlein A, Güllert S, Schmeisser C, Pommerening-Röser A, Grundhoff A, Daniel R, Hanelt D, Streit WR (2013) Metagenome survey of a multispecies and alga-associated biofilm revealed key elements of bacterial-algal interactions in photobioreactors. Appl Environ Microbiol 79:6196–6206. https://doi.org/10.1128/AEM.01641-13
Krohn-Molt I, Alawi M, Förstner KU, Wiegandt A, Burkhardt L, Indenbirken D, Thieß M, Grundhoff A, Kehr J, Tholey A, Streit WR (2017) Insights into microalga and bacteria interactions of selected phycosphere biofilms using metagenomic, transcriptomic, and proteomic approaches. Front Microbiol 8:1–14. https://doi.org/10.3389/fmicb.2017.01941
Lakshmi S, Kumar R, Rajendran S (2015) Automated system for identifying and recognizing rotifer contamination in Spirulina. Indian J Sci Technol 8:702–706. https://doi.org/10.17485/ijst/2015/v8i
Lane TW, Carney LT (2014) Title: parasites in algae mass culture. https://doi.org/10.3389/fmicb.2014.00278
Lee RE (2008) Basic characteristics of the algae. In: Phycology, Fourth ed. New York, pp 3–30
Lee Y-K, Shen H (2004) Basic Culturing Techniques. In: Amos Richmond (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Publishing Ltd, pp 40–56
Letcher PM, Lopez S, Schmieder R, Lee PA, Behnke C, Powell MJ, McBride RC (2013) Characterization of Amoeboaphelidium protococcarum, an algal parasite new to the Cryptomycota isolated from an outdoor algal pond used for the production of biofuel. PLoS One 8:e56232. https://doi.org/10.1371/journal.pone.0056232
Li W, Zhang T, Tang X, Wang B (2010) Oomycetes and fungi: important parasites on marine algae. Acta Oceanol Sin 29:74–81. https://doi.org/10.1007/s13131-010-0065-4
Lincoln EP, Hall TW, Koopman B (1983) Zooplankton control in mass algal cultures. Aquaculture 32:331–337. https://doi.org/10.1016/0044-8486(83)90230-2
López-Pacheco IY, Carrillo-Nieves D, Salinas-Salazar C, Silva-Núñez A, Arévalo-Gallegos A, Barceló D, Afewerki S, Iqbal HMN, Parra-Saldívar R (2019) Combination of nejayote and swine wastewater as a medium for Arthrospira maxima and Chlorella vulgaris production and wastewater treatment. Sci Total Environ 676:356–367. https://doi.org/10.1016/j.scitotenv.2019.04.278
Lopez-Rodas V, Agrelo M, Carrillo E, Ferrero LM, Larrauri A, MartÃn-Otero L, Costas E (2001) Resistance of microalgae to modern water contaminants as the result of rare spontaneous mutations. Eur J Phycol 36:179–190. https://doi.org/10.1017/S0967026201003109
Ma J, Xu L, Wang S, Zheng R, Jin S, Huang S, Huang Y (2002) Toxicity of 40 herbicides to the green alga Chlorella vulgaris. Ecotoxicol Environ Saf 51:128–132. https://doi.org/10.1006/eesa.2001.2113
Ma AT, Daniels EF, Gulizia N, Brahamsha B (2016) Isolation of diverse amoebal grazers of freshwater cyanobacteria for the development of model systems to study predator-prey interactions. Algal Res 13:85–93. https://doi.org/10.1016/j.algal.2015.11.010
Madigan MT, Martinko JM, Dunlap PV, Clark DP (2006) Microbiologia de Brock.pdf, 10th edn. PEARSON Prentince Hall, São Paulo
Magdouli S, Brar SK, Blais JF (2016) Co-culture for lipid production: advances and challenges. Biomass Bioenergy 92:20–30. https://doi.org/10.1016/j.biombioe.2016.06.003
Mahan KM, Odom OW, Herrin DL (2005) Controlling fungal contamination in Chlamydomonas reinhardtii cultures. Biotechniques 39:457–458. https://doi.org/10.2144/000112022
Mahmoud R, Ibrahim M, Ali G (2016) Closed photobioreactor for microalgae biomass production under indoor growth conditions. J Algal Biomass Util 7:86–92
McBride RC, Lopez S, Meenach C, Burnett M, Lee PA, Nohilly F, Behnke C (2014) Contamination management in low cost open algae ponds for biofuels production. Ind Biotechnol 10:221–227. https://doi.org/10.1089/ind.2013.0036
Melis A, Melnicki MR (2006) Integrated biological hydrogen production. Int J Hydrog Energy 31:1563–1573. https://doi.org/10.1016/j.ijhydene.2006.06.038
Méndez C, Uribe E, De Ciencias F, Católica U, Box PO, De Acuicultura D, De Ciencias F (2012) Control of Branchionus sp. and Amoeba sp. in cultures of Arthrospira sp. Lat Am J Aquat Res 40:553–561
Meseck SL (2007) Controlling the growth of a cyanobacterial contaminant, Synechoccus sp., in a culture of Tetraselmis chui (PLY429) by varying pH: implications for outdoor aquaculture production. Aquaculture 273:566–572. https://doi.org/10.1016/j.aquaculture.2007.10.043
Mishra AK, Pandey AB (1989) Toxicity of three herbicides to some nitrogen-fixing cyanobacteria. Ecotoxicol Environ Saf 17:236–246. https://doi.org/10.1016/0147-6513(89)90043-2
Moenne-Loccoz Y, Mavingui P, Combes C, Normand P, Steinberg C (2011) Microorganisms and biotic interactions. In: Bertrand J-C, Caumette P, Lebaron P, Matheron R, Philippe Normand TS-N (eds) Environmental microbiology: fundamentals and applications. Presses Universitaires de Pau et des Pays de l’Adour, p 933
Molina-Cárdenas CA, del Sánchez-Saavedra M P, Licea-Navarro AF (2016) Decreasing of bacterial content in Isochrysis galbana cultures by using some antibiotics. Rev Biol Mar Oceanogr 51:101–112
Moniz MBJ, Rindi F, Novis PM, Broady PA, Guiry MD (2012) Molecular phylogeny of antarctic Prasiola (prasiolales, trebouxiophyceae) reveals extensive cryptic diversity. J Phycol 48:940–955. https://doi.org/10.1111/j.1529-8817.2012.01172.x
Mooij PR, Stouten GR, van Loosdrecht MCM, Kleerebezem R (2015) Ecology-based selective environments as solution to contamination in microalgal cultivation. Curr Opin Biotechnol 33:46–51. https://doi.org/10.1016/j.copbio.2014.11.001
Moreno-Garrido I, Cañavate JP (2000) Assessing chemical compounds for controlling predator ciliates in outdoor mass cultures of the green algae Dunaliella salina. Aquac Eng 24:107–114. https://doi.org/10.1016/S0144-8609(00)00067-4
Nakamura K (1976) Fundamental studies on the physiology of rotifers in mass culture - v. dry. Aquaculture 8:301–307
Navajas-Benito EV, Alonso CA, Sanz S, Olarte C, Martínez-Olarte R, Hidalgo-Sanz S, Somalo S, CarmenTorres (2016) Molecular characterization of antibiotic resistance in Escherichia coli strains from a dairy cattle farm and its surroundings. J Sci Food Agric 2015–2018. https://doi.org/10.1002/jsfa.7709
Olaizola M (2003) Commercial development of microalgal biotechnology: from the test tube to the marketplace. Biomol Eng 20:459–466. https://doi.org/10.1016/S1389-0344(03)00076-5
Pareek A, Srivastava P (2016) Efficacy of antibiotics on bacterial contamination in outdoor cultures of Spirulina platensis. Algal Biomass 4:1–9
Park S (2014) The selective use of chlorine to inhibit algal predators and avoid pond crashes for the algae-biodiesel industry
Peng L, Lan CQ, Zhang Z, Sarch C, Laporte M (2015) Control of protozoa contamination and lipid accumulation in Neochloris oleoabundans culture: effects of pH and dissolved inorganic carbon. Bioresour Technol 197:143–151. https://doi.org/10.1016/j.biortech.2015.07.101
Peniuk GT, Schnurr PJ, Allen DG (2016) Identification and quantification of suspended algae and bacteria populations using flow cytometry: applications for algae biofuel and biochemical growth systems. J Appl Phycol 28:95–104. https://doi.org/10.1007/s10811-015-0569-6
Post FJ, Borowitzka LJ, Borowitzka MA, Mackay B, Moulton T (1983) The protozoa of a Western Australian hypersaline lagoon. Hydrobiologia 105:95–113. https://doi.org/10.1007/BF00025180
Qi Z, Shi B, Hu Z, Zhang Y, Wu W (2011) Ultrastructural effects of Celangulin V on midgut cells of the oriental armyworm, Mythimna separata walker (Lepidoptera: Noctuidae). Ecotoxicol Environ Saf 74:439–444. https://doi.org/10.1016/j.ecoenv.2010.10.004
Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003
Rasconi S, Jobard M, Jouve L, Sime-Ngando T (2009) Use of calcofluor white for detection, identification, and quantification of phytoplanktonic fungal parasites. Appl Environ Microbiol 75:2545–2553. https://doi.org/10.1128/AEM.02211-08
Rego D, Costa L, Pereira MT, Redondo LM (2015a) Cell membrane permeabilization studies of Chlorella sp. by pulsed electric fields. IEEE Trans Plasma Sci 43:3483–3488. https://doi.org/10.1109/TPS.2015.2448660
Rego D, Redondo LM, Geraldes V, Costa L, Navalho J, Pereira MT (2015b) Control of predators in industrial scale microalgae cultures with pulsed electric fields. Bioelectrochemistry 103:60–64. https://doi.org/10.1016/j.bioelechem.2014.08.004
Ren HY, Liu BF, Kong F, Zhao L, Ren NQ (2015) Improved Nile red staining of Scenedesmus sp. by combining ultrasonic treatment and three-dimensional excitation emission matrix fluorescence spectroscopy. Algal Res 7:11–15. https://doi.org/10.1016/j.algal.2014.11.007
Richardson JW, Johnson MD, Zhang X, Zemke P, Chen W, Hu Q (2014) A financial assessment of two alternative cultivation systems and their contributions to algae biofuel economic viability. Algal Res 4:96–104. https://doi.org/10.1016/j.algal.2013.12.003
Richmond CA, Wagener K, Rebello ADL (1987) Production of Spirulina and other microalgae. Hydrobiologia 70:1987
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. https://doi.org/10.1099/00221287-111-1-1
Roncero C, Duran A (1985) Effect of Calcofluor white and Congo red on fungal cell wall morphogenesis : in vivo activation of chitin polymerization. J Bacteriol 163:1180–1185
Roth BL, Poot M, Yue ST, Millard PJ, Roth BL, Poot M, Yue ST, Millard PJ (1997) Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl Environ Microbiol 63:2421–2431
Salvesen I, Reitan KI, Skjermo J, Øie G (2000) Microbial environments in marine larviculture: impacts of algal growth rates on the bacterial load in six microalgae. Aquac Int 8:275–287. https://doi.org/10.1023/A:1009200926452
Saulis G (2010) Electroporation of cell membranes: the fundamental effects of pulsed electric fields in food processing. Food Eng Rev 2:52–73. https://doi.org/10.1007/s12393-010-9023-3
Shin W, Boo SM, Longcore JE (2001) Entophlyctis apiculata, a chytrid parasite of Chlamydomonas sp. (Chlorophyceae). Can J Bot 79:1083–1089. https://doi.org/10.1139/cjb-79-9-1083
Shunyu S, Yongding L, Yinwu S, Genbao L, Dunhai L (2006) Lysis of Aphanizomenon flos-aquae (Cyanobacterium) by a bacterium Bacillus cereus. Biol Control 39:345–351. https://doi.org/10.1016/j.biocontrol.2006.06.011
Sieracki CK, Sieracki ME, Yentsch CS (1998) An imaging-in-flow system for automated analysis of marine microplankton. Mar Ecol Prog Ser 168:285–296. https://doi.org/10.3354/meps168285
Simon C, Daniel R (2011) MINIREVIEW Metagenomic analyses : past and future trends. Appl Env 77:1153–1161. https://doi.org/10.1128/AEM.02345-10
Singh G, Marimuthu P, De Heluani CS, Catalan CAN (2006) Antioxidant and biocidal activities of Carum nigrum (Seed) essential oil, oleoresin, and their selected components. J Agric Food Chem 54:174–181. https://doi.org/10.1021/jf0518610
Sosa-Hernández J, Romero-Castillo K, Parra-Arroyo L, Aguilar-Aguila-Isaías MA, García-Reyes IE, Ahmed I, Parra-Saldivar R, Bilal M, Iqbal HMN (2019) Mexican microalgae biodiversity and state-of-the-art extraction strategies to meet sustainable circular economy challenges : high-value compounds and their applied perspectives. Mar Drugs 17(3):174. https://doi.org/10.3390/md17030174
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96. https://doi.org/10.1263/jbb.101.87
Srivastava BS (1970) Sensitivity and resistance of a blue-green alga Phormidium mucicola to streptomycin and penicillin. Arch Mikrobiol 72:182–185. https://doi.org/10.1007/BF00409523
Stephenson AL, Kazamia E, Dennis JS, Howe CJ, Scott SA, Smith AG (2010) Life-cycle assessment of potential algal biodiesel production in the united kingdom: a comparison of raceways and air-lift tubular bioreactors. Energy Fuel 24:4062–4077. https://doi.org/10.1021/ef1003123
Tate JJ, Gutierrez-Wing MT, Rusch KA, Benton MG (2013) The effects of plant growth substances and mixed cultures on growth and metabolite production of green algae Chlorella sp.: a review. J Plant Growth Regul 32:417–428. https://doi.org/10.1007/s00344-012-9302-8
Twiner MJ, Chidiac P, Dixon SJ, Trick CG (2005) Extracellular organic compounds from the ichthyotoxic red tide alga Heterosigma akashiwo elevate cytosolic calcium and induce apoptosis in Sf9 cells. Harmful Algae 4:789–800. https://doi.org/10.1016/j.hal.2004.12.006
Ugwu CU, Aoyagi H, Uchiyama H (2008) Photobioreactors for mass cultivation of algae. Bioresour Technol 99:4021–4028. https://doi.org/10.1016/j.biortech.2007.01.046
Van Ginkel SW, Bidwell M, Igou T, Gijon-Felix R, Salvi EJNR, De Oliveira SHR, Duarte LHK, Steiner D, Hu Z, Johnston R, Snell T, Chen Y (2016) The prevention of saltwater algal pond contamination using the electron transport chain disruptor, rotenone. Algal Res 18:209–212. https://doi.org/10.1016/j.algal.2016.06.012
Van Vuuren J, Pierterse A, Jacobs A, Steynberg M (1998) Different Counting Methods for Algal Studies. In: Conference: Biennial Conference of the Water Institute of Southern Africa
Van Wichelen J, van Gremberghe I, Vanormelingen P, Debeer AE, Leporcq B, Menzel D, Codd GA, Descy JP, Vyverman W (2010) Strong effects of amoebae grazing on the biomass and genetic structure of a Microcystis bloom (Cyanobacteria). Environ Microbiol 12:2797–2813. https://doi.org/10.1111/j.1462-2920.2010.02249.x
Vaz MGMV, Bastos RW, Milanez GP, Moura MN, Ferreira EG, Perin C, Pontes MCF, do Nascimento AG (2014) Use of sodium hypochlorite solutions to obtain axenic cultures of Nostoc strains (Cyanobacteria). Rev Bras Bot 37:115–120. https://doi.org/10.1007/s40415-014-0055-4
Vázquez-Martínez G, Rodriguez MH, Hernández-Hernández F, Ibarra JE (2004) Strategy to obtain axenic cultures from field-collected samples of the cyanobacterium Phormidium animalis. J Microbiol Methods 57:115–121. https://doi.org/10.1016/j.mimet.2003.12.003
Vu CHT, Lee HG, Chang YK, Oh HM (2018) Axenic cultures for microalgal biotechnology: establishment, assessment, maintenance, and applications. Biotechnol Adv 36:380–396. https://doi.org/10.1016/j.biotechadv.2017.12.018
Wahi N, Bhatia AK, Bhadauria S (2018) Impact of protozoan Vahlkampfia sp. on the growth of algae Chlorella vulgaris glamtr. J Environ Biol 39:109–115. https://doi.org/10.22438/jeb/39/1/MRN-663
Wang B, Lan CQ, Horsman M (2012) Closed photobioreactors for production of microalgal biomasses. Biotechnol Adv 30:904–912. https://doi.org/10.1016/j.biotechadv.2012.01.019
Wang H, Zhang W, Chen L, Wang J, Liu T (2013) The contamination and control of biological pollutants in mass cultivation of microalgae. Bioresour Technol 128:745–750. https://doi.org/10.1016/j.biortech.2012.10.158
Watanabe K, Takihana N, Aoyagi H, Hanada S, Watanabe Y, Ohmura N, Saiki H, Tanaka H (2005) Symbiotic association in Chlorella culture. FEMS Microbiol Ecol 51:187–196. https://doi.org/10.1016/j.femsec.2004.08.004
Weaver JL (2000) Introduction to flow cytometry. Methods 3(21):199–201
Whitton R, Le Mével A, Pidou M, Ometto F, Villa R, Jefferson B (2016) Influence of microalgal N and P composition on wastewater nutrient remediation. Water Res 91:371–378. https://doi.org/10.1016/j.watres.2015.12.054
Wrede D, Taha M, Miranda AF, Kadali K, Stevenson T, Ball AS, Mouradov A (2014) Co-cultivation of fungal and microalgal cells as an efficient system for harvesting microalgal cells, lipid production and wastewater treatment. PLoS One 9:e113497. https://doi.org/10.1371/journal.pone.0113497
Wu S, Li X, Yu J, Wang Q (2012) Increased hydrogen production in co-culture of Chlamydomonas reinhardtii and Bradyrhizobium japonicum. Bioresour Technol 123:184–188. https://doi.org/10.1016/j.biortech.2012.07.055
Xinyao L, Miao S, Yonghong L, Yin G, Zhongkai Z, Donghui W, Weizhong W, Chencai A (2006) Feeding characteristics of an amoeba (Lobosea: Naegleria) grazing upon cyanobacteria: food selection, ingestion and digestion progress. Microb Ecol 51:315–325. https://doi.org/10.1007/s00248-006-9031-2
Yamane K, Matsuyama S, Igarashi K, Utsumi M, Shiraiwa Y, Kuwabara T (2013) Anaerobic coculture of microalgae with Thermosipho globiformans and Methanocaldococcus jannaschii at 68°C enhances generation of n alkane rich biofuels after pyrolysis. Appl Environ Microbiol 79:924–930. https://doi.org/10.1128/AEM.01685-12
Yu X, Zheng Y, Dorgan KM, Chen S (2011) Oil production by oleaginous yeasts using the hydrolysate from pretreatment of wheat straw with dilute sulfuric acid. Bioresour Technol 102:6134–6140. https://doi.org/10.1016/j.biortech.2011.02.081
Yu H, Kim J, Lee C (2019) Potential of mixed-culture microalgae enriched from aerobic and anaerobic sludges for nutrient removal and biomass production from anaerobic effluents. Bioresour Technol 280:325–336. https://doi.org/10.1016/j.biortech.2019.02.054
Yuan X, Kumar A, Sahu AK, Ergas SJ (2011) Impact of ammonia concentration on Spirulina platensis growth in an airlift photobioreactor. Bioresour Technol 102:3234–3239. https://doi.org/10.1016/j.biortech.2010.11.019
Zapalski MK (2011) Is absence of proof a proof of absence? Comments on commensalism. Palaeogeogr Palaeoclimatol Palaeoecol 302:484–488. https://doi.org/10.1016/j.palaeo.2011.01.013
Zbinden MDA, Sturm BSM, Nord RD, Carey WJ, Moore D, Shinogle H, Stagg-Williams SM (2013) Pulsed electric field (PEF) as an intensification pretreatment for greener solvent lipid extraction from microalgae. Biotechnol Bioeng 110:1605–1615. https://doi.org/10.1002/bit.24829
Zhang C, Zhang Y, Zhuang B, Zhou X (2014) Strategic enhancement of algal biomass, nutrient uptake and lipid through statistical optimization of nutrient supplementation in coupling Scenedesmus obliquus-like microalgae cultivation and municipal wastewater treatment. Bioresour Technol 171:71–79. https://doi.org/10.1016/j.biortech.2014.07.060
Zhou D, Li Y, Yang Y, Wang Y, Zhang C, Wang D (2014) Granulation, control of bacterial contamination, and enhanced lipid accumulation by driving nutrient starvation in coupled wastewater treatment and Chlorella regularis cultivation. Appl Microbiol Biotechnol 99:1531–1541. https://doi.org/10.1007/s00253-014-6288-0
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This research was funded by CNPq, the Brazilian National Council for Scientific and Technological Development, grant number 407543/2013-0, and CAPES, the Coordination of Improvement of Higher Education Personnel - PROEX program.
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Molina, D., de Carvalho, J.C., Júnior, A.I.M. et al. Biological contamination and its chemical control in microalgal mass cultures. Appl Microbiol Biotechnol 103, 9345–9358 (2019). https://doi.org/10.1007/s00253-019-10193-7
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DOI: https://doi.org/10.1007/s00253-019-10193-7