Applied Microbiology and Biotechnology

, Volume 103, Issue 23–24, pp 9345–9358 | Cite as

Biological contamination and its chemical control in microalgal mass cultures

  • Denisse Molina
  • Júlio Cesar de CarvalhoEmail author
  • Antônio Irineudo Magalhães Júnior
  • Craig Faulds
  • Emmanuel Bertrand
  • Carlos Ricardo Soccol


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.


Microalgae Contamination Mass cultures Algal parasites Control 


Funding information

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.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abeliovich A, Dikbuck S (1977) Factors Affecting Infection of Scenedesmus obliquus by a Chytridium sp. in Sewage Oxidation Ponds. Appl Environ Microbiol 34:832–836Google Scholar
  2. 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. Google Scholar
  3. 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 46:223–229CrossRefGoogle Scholar
  4. 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. CrossRefPubMedGoogle Scholar
  5. Amaral R, Pereira JC, Pais AACC, Santos LMA (2013) Is axenicity crucial to cryopreserve microalgae? Cryobiology 67:312–320. CrossRefPubMedGoogle Scholar
  6. 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. CrossRefPubMedGoogle Scholar
  7. Anderson RA (2005) Algal culturing techniques, 1st ednGoogle Scholar
  8. 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. CrossRefPubMedGoogle Scholar
  9. 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. CrossRefPubMedGoogle Scholar
  10. Azov Y, Goldman JC (1982) Free ammonia inhibition of algal photosynthesis in intensive cultures. Appl Environ Microbiol 43:735–739PubMedPubMedCentralGoogle Scholar
  11. 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. CrossRefGoogle Scholar
  12. Benson (2001) Microbiological applications lab manual. The McGraw-Hill Companies, 8th EdGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. 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. CrossRefPubMedGoogle Scholar
  15. 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 155Google Scholar
  16. 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. CrossRefPubMedGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. 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. CrossRefPubMedGoogle Scholar
  19. 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. CrossRefPubMedGoogle Scholar
  20. 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. CrossRefPubMedGoogle Scholar
  21. Cole J (1994) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13 (1):291–314CrossRefGoogle Scholar
  22. 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. CrossRefGoogle Scholar
  23. Davies J, Davies D (2010) Origins and Evolution of Antibiotic Resistance. Microbiol Mol Biol Rev 74:417–433. CrossRefGoogle Scholar
  24. Day JG, Thomas NJ, Achilles-Day UEM, Leakey RJG (2012) Early detection of protozoan grazers in algal biofuel cultures. Bioresour Technol 114:715–719. CrossRefPubMedGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. 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 31:359–365CrossRefGoogle Scholar
  27. 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. CrossRefPubMedGoogle Scholar
  28. Dryden RC, Wright SJL (1984) Predation of cyanobacteria by protoza. J Protozool 31:A42–A43Google Scholar
  29. 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. CrossRefGoogle Scholar
  30. Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50. CrossRefPubMedGoogle Scholar
  31. 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. CrossRefPubMedGoogle Scholar
  32. 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. CrossRefPubMedGoogle Scholar
  33. Fulbright SP, Dean MK, Wardle G, Lammers PJ, Chisholm S (2014) Molecular diagnostics for monitoring contaminants in algal cultivation. Algal Res 4:41–51. CrossRefGoogle Scholar
  34. 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. CrossRefPubMedGoogle Scholar
  35. 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. CrossRefGoogle Scholar
  36. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 66:1527–1531CrossRefGoogle Scholar
  40. 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. CrossRefPubMedGoogle Scholar
  41. Grahl T, Märkl H (1996) Killing of micro-organisms by pulsed electric fields. Appl Microbiol Biotechnol 45:148–157CrossRefGoogle Scholar
  42. 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. CrossRefGoogle Scholar
  43. Guerrini F, Mazzotti A, Boni L, Pistocchi R (1998) Bacterial-algal interaction in polysaccharide production. Aquat Microb Ecol 15:247–253. CrossRefGoogle Scholar
  44. Guillard RRL (2005) Purification methods for microalgae. In: Algal culturing techniques. Elsevier Academic Press USA, Cambridge, pp 117–132Google Scholar
  45. 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. CrossRefGoogle Scholar
  46. Gutterman Y (1994) Algal allelopathy. Bot Rev 60:373–425CrossRefGoogle Scholar
  47. 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. CrossRefGoogle Scholar
  48. 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. CrossRefGoogle Scholar
  49. Haraguchi L, Jakobsen HH, Lundholm N, Carstensen J (2018) Phytoplankton community dynamic: a driver for ciliate trophic strategies. Front Mar Sci 5:1–16. CrossRefGoogle Scholar
  50. Harrison DEF (1978) Mixed cultures in industrial fermentation processes. Adv Appl Microbiol 24:129–164. CrossRefGoogle Scholar
  51. 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. CrossRefGoogle Scholar
  52. Hess S, Sausen N, Melkonian M (2012) Shedding light on vampires: the phylogeny of vampyrellid amoebae revisited. PLoS One 7:e31165. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Hesseltine CW et al (1992) Mixed-culture fermentations. In: Application of biotechnology for traditional fermented foods. National Academy Press, Washington D.C., pp 52–58Google Scholar
  54. 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. CrossRefGoogle Scholar
  55. 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. CrossRefPubMedGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. 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. CrossRefPubMedGoogle Scholar
  58. 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. CrossRefGoogle Scholar
  59. 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. CrossRefGoogle Scholar
  60. 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. CrossRefGoogle Scholar
  61. Kalia AMR (2011) Bioaugmentation, biostimulation and biocontrol. In: Ajay S, Kuhad NPRC (eds) Bioaugmentation, bioestimulation and biocontrol. Springer, Berlin, pp 223–240CrossRefGoogle Scholar
  62. 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. CrossRefGoogle Scholar
  63. 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. CrossRefGoogle Scholar
  64. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  65. 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. CrossRefGoogle Scholar
  66. Lakshmi S, Kumar R, Rajendran S (2015) Automated system for identifying and recognizing rotifer contamination in Spirulina. Indian J Sci Technol 8:702–706. CrossRefGoogle Scholar
  67. Lane TW, Carney LT (2014) Title: parasites in algae mass culture.
  68. Lee RE (2008) Basic characteristics of the algae. In: Phycology, Fourth ed. New York, pp 3–30Google Scholar
  69. 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 40–56Google Scholar
  70. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Li W, Zhang T, Tang X, Wang B (2010) Oomycetes and fungi: important parasites on marine algae. Acta Oceanol Sin 29:74–81. CrossRefGoogle Scholar
  72. Lincoln EP, Hall TW, Koopman B (1983) Zooplankton control in mass algal cultures. Aquaculture 32:331–337. CrossRefGoogle Scholar
  73. 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. CrossRefPubMedGoogle Scholar
  74. 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. CrossRefGoogle Scholar
  75. 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. CrossRefPubMedGoogle Scholar
  76. 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. CrossRefGoogle Scholar
  77. Madigan MT, Martinko JM, Dunlap PV, Clark DP (2006) Microbiologia de Brock.pdf, 10th edn. PEARSON Prentince Hall, São PauloGoogle Scholar
  78. Magdouli S, Brar SK, Blais JF (2016) Co-culture for lipid production: advances and challenges. Biomass Bioenergy 92:20–30. CrossRefGoogle Scholar
  79. Mahan KM, Odom OW, Herrin DL (2005) Controlling fungal contamination in Chlamydomonas reinhardtii cultures. Biotechniques 39:457–458. CrossRefPubMedGoogle Scholar
  80. Mahmoud R, Ibrahim M, Ali G (2016) Closed photobioreactor for microalgae biomass production under indoor growth conditions. J Algal Biomass Util 7:86–92Google Scholar
  81. 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. CrossRefGoogle Scholar
  82. Melis A, Melnicki MR (2006) Integrated biological hydrogen production. Int J Hydrog Energy 31:1563–1573. CrossRefGoogle Scholar
  83. 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 40:553–561CrossRefGoogle Scholar
  84. 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. CrossRefGoogle Scholar
  85. Mishra AK, Pandey AB (1989) Toxicity of three herbicides to some nitrogen-fixing cyanobacteria. Ecotoxicol Environ Saf 17:236–246. CrossRefPubMedGoogle Scholar
  86. 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 933Google Scholar
  87. 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 51:101–112CrossRefGoogle Scholar
  88. 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. CrossRefPubMedGoogle Scholar
  89. 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. CrossRefPubMedGoogle Scholar
  90. 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. CrossRefGoogle Scholar
  91. Nakamura K (1976) Fundamental studies on the physiology of rotifers in mass culture - v. dry. Aquaculture 8:301–307CrossRefGoogle Scholar
  92. 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. CrossRefGoogle Scholar
  93. Olaizola M (2003) Commercial development of microalgal biotechnology: from the test tube to the marketplace. Biomol Eng 20:459–466. CrossRefPubMedGoogle Scholar
  94. Pareek A, Srivastava P (2016) Efficacy of antibiotics on bacterial contamination in outdoor cultures of Spirulina platensis. Algal Biomass 4:1–9Google Scholar
  95. Park S (2014) The selective use of chlorine to inhibit algal predators and avoid pond crashes for the algae-biodiesel industryGoogle Scholar
  96. 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. CrossRefPubMedGoogle Scholar
  97. 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. CrossRefGoogle Scholar
  98. Post FJ, Borowitzka LJ, Borowitzka MA, Mackay B, Moulton T (1983) The protozoa of a Western Australian hypersaline lagoon. Hydrobiologia 105:95–113. CrossRefGoogle Scholar
  99. 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. CrossRefGoogle Scholar
  100. Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29. CrossRefPubMedGoogle Scholar
  101. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  102. 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. CrossRefGoogle Scholar
  103. 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. CrossRefPubMedGoogle Scholar
  104. 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. CrossRefGoogle Scholar
  105. 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. CrossRefGoogle Scholar
  106. Richmond CA, Wagener K, Rebello ADL (1987) Production of Spirulina and other microalgae. Hydrobiologia 70:1987Google Scholar
  107. 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. CrossRefGoogle Scholar
  108. 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 163:1180–1185PubMedPubMedCentralGoogle Scholar
  109. 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 63:2421–2431PubMedPubMedCentralGoogle Scholar
  110. 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. CrossRefGoogle Scholar
  111. Saulis G (2010) Electroporation of cell membranes: the fundamental effects of pulsed electric fields in food processing. Food Eng Rev 2:52–73. CrossRefGoogle Scholar
  112. Shin W, Boo SM, Longcore JE (2001) Entophlyctis apiculata, a chytrid parasite of Chlamydomonas sp. (Chlorophyceae). Can J Bot 79:1083–1089. CrossRefGoogle Scholar
  113. 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. CrossRefGoogle Scholar
  114. 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. CrossRefGoogle Scholar
  115. Simon C, Daniel R (2011) MINIREVIEW Metagenomic analyses : past and future trends. Appl Env 77:1153–1161. CrossRefGoogle Scholar
  116. 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. CrossRefGoogle Scholar
  117. 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. CrossRefPubMedCentralGoogle Scholar
  118. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96. CrossRefPubMedGoogle Scholar
  119. Srivastava BS (1970) Sensitivity and resistance of a blue-green alga Phormidium mucicola to streptomycin and penicillin. Arch Mikrobiol 72:182–185. CrossRefPubMedGoogle Scholar
  120. 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. CrossRefGoogle Scholar
  121. 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. CrossRefGoogle Scholar
  122. 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. CrossRefGoogle Scholar
  123. Ugwu CU, Aoyagi H, Uchiyama H (2008) Photobioreactors for mass cultivation of algae. Bioresour Technol 99:4021–4028. CrossRefPubMedGoogle Scholar
  124. 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. CrossRefGoogle Scholar
  125. 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 AfricaGoogle Scholar
  126. 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. CrossRefPubMedGoogle Scholar
  127. 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. CrossRefGoogle Scholar
  128. 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. CrossRefPubMedGoogle Scholar
  129. Vu CHT, Lee HG, Chang YK, Oh HM (2018) Axenic cultures for microalgal biotechnology: establishment, assessment, maintenance, and applications. Biotechnol Adv 36:380–396. CrossRefPubMedGoogle Scholar
  130. 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. CrossRefGoogle Scholar
  131. Wang B, Lan CQ, Horsman M (2012) Closed photobioreactors for production of microalgal biomasses. Biotechnol Adv 30:904–912. CrossRefPubMedGoogle Scholar
  132. 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. CrossRefPubMedGoogle Scholar
  133. 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. CrossRefPubMedGoogle Scholar
  134. Weaver JL (2000) Introduction to flow cytometry. Methods 3(21):199–201CrossRefGoogle Scholar
  135. 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. CrossRefPubMedGoogle Scholar
  136. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  137. 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. CrossRefPubMedGoogle Scholar
  138. 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. CrossRefPubMedGoogle Scholar
  139. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  140. 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. CrossRefPubMedGoogle Scholar
  141. 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. CrossRefPubMedGoogle Scholar
  142. 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. CrossRefPubMedGoogle Scholar
  143. Zapalski MK (2011) Is absence of proof a proof of absence? Comments on commensalism. Palaeogeogr Palaeoclimatol Palaeoecol 302:484–488. CrossRefGoogle Scholar
  144. 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. CrossRefPubMedGoogle Scholar
  145. 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. CrossRefPubMedGoogle Scholar
  146. 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. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Bioprocess Engineering and BiotechnologyFederal University of ParanáCuritibaBrazil
  2. 2.Polytech Marseille, UMR 1163 Biotechnologie des Champignons FilamenteuxAix-Marseille UniversitéMarseille Cedex 09France

Personalised recommendations