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Soil algae enzymes and their biotechnological applications

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Abstract

At present time, most of the enzymes are derived from biological sources, including plants, animals, microalgae, algae, and other microorganisms. Microorganism enzymes, among the others, account for the biggest part of application and demand in industries. These enzymes from soil microorganisms are very essential not only for soil fertility but also for biotechnological significance. Soil enzymes from microalage, comprising Amylase, Carbonic anhydrase, Galactosidase, Laccase, L-Asparaginase, Lipase, Peroxidase, Phytase, Protease, and Superoxide dismutase attract a considerable amount of attention for themselves in various industries. Most of the enzymes mentioned above have a great potential for their application in biotechnology and agriculture. Majority of such enzymes are known for their versatility and countless applications in various fields; thus, performing research on these enzymes in the future would be auspicious. This review paper presents an overview of the potential of soil algae enzymes in fields like biotechnology, medicine and agriculture, and also provides areas for advancement in researches related to this field.

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References

  1. Tiffany LH. Ecology of freshwater algae. In: Smith GM, editor. Manual of phycology. Waltham: Chronica Botanica Co.; 1951.

    Google Scholar 

  2. Levi C, Gibbs M. Starch degradation in synchronously grown Chlamydomonas reinhardtii and characterization of the amylase. Plant Physiol. 1984;74:459–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kombrink E, Wöber G. Identification and subcellular localization of starch-metabolizing enzymes in the green alga Dunaliella marina. Planta. 1980;149:130–7.

    Article  CAS  PubMed  Google Scholar 

  4. Manoj B, Sushma Chavan M. Western Ghats terrestrial microalgae serve as a source of amylase and antioxidants enzymes. J Pharmacogn Phytochem. 2018;7:1555–60.

    Article  CAS  Google Scholar 

  5. Patil KJ, Mahajan R. Enzymatic study of fresh water macro and micro algae isolated from Jalgaon, Maharashtra. Int J Pharma Bio Sci. 2016;7:207–15.

    CAS  Google Scholar 

  6. Swarnalatha G, Hegde NS, Chauhan VS, Sarada R. The effect of carbon dioxide rich environment on carbonic anhydrase activity, growth and metabolite production in indigenous freshwater microalgae. Algal Res. 2015;9:151–9.

    Article  Google Scholar 

  7. Badger MR, Price GD. CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot. 2003;54:609–22.

    Article  CAS  PubMed  Google Scholar 

  8. Dionisio-Sese ML, Miyachi S. The effect of sodium chloride on carbonic anhydrase activity in marine microalgae 1. J Phycol. 1992;28:619–24.

    Article  CAS  Google Scholar 

  9. Dey P, Kauss H. α-galactosidase of Poterioochromonas malhamensis. Phytochemistry. 1981;20:45–8.

    Article  CAS  Google Scholar 

  10. Suwal S, Bentahar J, Marciniak A, Beaulieu L, Deschênes J-S, Doyen A. Evidence of the production of galactooligosaccharide from whey permeate by the microalgae Tetradesmus obliquus. Algal Res. 2019;39:101470.

    Article  Google Scholar 

  11. Zanette CM, Mariano AB, Yukawa YS, Mendes I, Spier MR. Microalgae mixotrophic cultivation for β-galactosidase production. J Appl Phycol. 2019;31:1597–606.

    Article  CAS  Google Scholar 

  12. Bentahar J, Doyen A, Beaulieu L, Deschênes J-S. Investigation of β-galactosidase production by microalga Tetradesmus obliquus in determined growth conditions. J Appl Phycol. 2019;31:301–8.

    Article  CAS  Google Scholar 

  13. Girard J-M, Roy M-L, Hafsa MB, Gagnon J, Faucheux N, Heitz M, Tremblay R, Deschênes J-S. Mixotrophic cultivation of green microalgae Scenedesmus obliquus on cheese whey permeate for biodiesel production. Algal Res. 2014;5:241–8.

    Article  Google Scholar 

  14. Davies CM, Apte SC, Peterson SM, Stauber JL. Plant and algal interference in bacterial beta-d-galactosidase and beta-d-glucuronidase assays. Appl Environ Microbiol. 1994;60:3959–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Otto B, Schlosser D, Reisser W. First description of a laccase-like enzyme in soil algae. Arch Microbiol. 2010;192:759–68.

    Article  CAS  PubMed  Google Scholar 

  16. Otto B, Beuchel C, Liers C, Reisser W, Harms H, Schlosser D. Laccase-like enzyme activities from chlorophycean green algae with potential for bioconversion of phenolic pollutants. FEMS Microbiol Lett. 2015;362:11.

    Article  CAS  Google Scholar 

  17. Afreen S, Shamsi TN, Baig MA, Ahmad N, Fatima S, Qureshi MI, Hassan MI, Fatma T. A novel multicopper oxidase (laccase) from cyanobacteria: purification, characterization with potential in the decolorization of anthraquinonic dye. PLoS ONE. 2017;12:e0175144.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Paul JH, Cooksey KE. Asparagine metabolism and asparaginase activity in a euryhaline Chlamydomonas species. Can J Microbiol. 1979;25:1443–51.

    Article  CAS  PubMed  Google Scholar 

  19. Ebrahiminezhad A, Rasoul-Amini S, Ghoshoon MB, Ghasemi Y. Chlorella vulgaris, a novel microalgal source for L-asparaginase production. Biocatal Agric Biotechnol. 2014;3:214–7.

    Article  Google Scholar 

  20. Prihanto AA, Wakayama M. Combination of environmental stress and localization of l-asparaginase in Arthrospira platensis for production improvement. 3 Biotech. 2014;4:647–53.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Abd El Baky HH, El Baroty GS (2016): Optimization of growth conditions for purification and production of L-asparaginase by Spirulina maxima. Evid Based Complement Alternat Med 2016

  22. Kebeish R, El-Sayed A, Fahmy H, Abdel-Ghany A. Molecular cloning, biochemical characterization, and antitumor properties of a novel L-asparaginase from Synechococcus elongatus PCC6803. Biochem Mosc. 2016;81:1173–81.

    Article  CAS  Google Scholar 

  23. Yong SK, Lim BH, Saleh S, Tey L-H. Optimisation, purification and characterisation of extracellular lipase from Botryococcus sudeticus (UTEX 2629). J Mol Catal B Enzym. 2016;126:99–105.

    Article  CAS  Google Scholar 

  24. Savvidou MG, Sotiroudis TG, Kolisis FN. Cell surface and cellular debris-associated heat-stable lipolytic enzyme activities of the marine alga Nannochloropsis oceanica. Biocatal Biotransform. 2016;34:24–32.

    Article  CAS  Google Scholar 

  25. Godet S, Hérault J, Pencreac’h G, Ergan F, Loiseau C. Isolation and analysis of a gene from the marine microalga Isochrysis galbana that encodes a lipase-like protein. J Appl Phycol. 2012;24:1547–53.

    Article  CAS  Google Scholar 

  26. Hubert F, Poisson L, Loiseau C, Gauvry L, Pencréac’h G, Hérault J, Ergan F. Lipids and lipolytic enzymes of the microalga Isochrysis galbana. Les Ulis: EDP Sciences; 2017.

    Book  Google Scholar 

  27. Baldev E, MubarakAli D, Ilavarasi A, Pandiaraj D, Ishack KSS, Thajuddin N. Degradation of synthetic dye, Rhodamine B to environmentally non-toxic products using microalgae. Colloids Surf B. 2013;105:207–14.

    Article  CAS  Google Scholar 

  28. Oesterhelt C, Vogelbein S, Shrestha R, Stanke M, Weber A. The genome of the thermoacidophilic red microalga Galdieria sulphuraria encodes a small family of secreted class III peroxidases that might be involved in cell wall modification. Planta. 2008;227:353–62.

    Article  CAS  PubMed  Google Scholar 

  29. Murphy CD, Moore RM, White RL. Peroxidases from marine microalgae. J Appl Phycol. 2000;12:507–13.

    Article  CAS  Google Scholar 

  30. Overbaugh JM, Fall R. Characterization of a selenium-independent glutathione peroxidase from Euglena gracilis. Plant Physiol. 1985;77:437–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Klanbut K, Peerapornpisarn Y, Khanongnuch C, Ishii M. Phytase from some strains of thermophilic blue-green algae. Jpn J Phycol. 2004;2:57–60.

    Google Scholar 

  32. Nanni B, Balestreri E, Dainese E, Cozzani I, Felicioli R. Characterisation of a specific phycocyanin-hydrolysing protease purified from Spirulina platensis. Microbiol Res. 2001;156:259–66.

    Article  CAS  PubMed  Google Scholar 

  33. Yada E, Nagata H, Noguchi Y, Kodera Y, Nishimura H, Inada Y, Matsushima A. An arginine specific protease from Spirulina platensis. Mar Biotechnol. 2005;7:474–80.

    Article  CAS  Google Scholar 

  34. Maldener I, Lockau W, Cai Y, Wolk CP. Calcium-dependent protease of the cyanobacterium Anabaena: molecular cloning and expression of the gene in Escherichia coli, sequencing and site-directed mutagenesis. Mol Gen Genet MGG. 1991;225:113–20.

    Article  CAS  PubMed  Google Scholar 

  35. Lockau W, Massalsky B, Dirmeier A. Purification and partial characterization of a calcium-stimulated protease from the cyanobacterium, Anabaena variabilis. Eur J Biochem. 1988;172:433–8.

    Article  CAS  PubMed  Google Scholar 

  36. Páblo E, de Souza F, de Barros R, Marques D, Porto A, Bezerra R. Enhanced production of fibrinolytic protease from microalgae Chlorella vulgaris using glycerol and corn steep liquor as nutrient. Ann Microbiol Res. 2017;1:9–19.

    Google Scholar 

  37. Guzmán-Murillo MA, López-Bolaños CC, Ledesma-Verdejo T, Roldan-Libenson G, Cadena-Roa MA, Ascencio F. Effects of fertilizer-based culture media on the production of exocellular polysaccharides and cellular superoxide dismutase by Phaeodactylum tricornutum (Bohlin). J Appl Phycol. 2007;19:33–41.

    Article  CAS  Google Scholar 

  38. Gunes S, Tamburaci S, Imamoglu E, Dalay MC. Determination of superoxide dismutase activities in different cyanobacteria for scavenging of reactive oxygen species. J Biol Act Prod Nat. 2015;5:25–32.

    CAS  Google Scholar 

  39. Canini A, Civitareale P, Marini S, Caiola MG, Rotilio G. Purification of iron superoxide dismutase from the cyanobacterium Anabaena cylindrica Lemm. and localization of the enzyme in heterocysts by immunogold labeling. Planta. 1992;187:438–44.

    Article  CAS  PubMed  Google Scholar 

  40. Misra H, Fridovich I. Purification and properties of superoxide dismutase from a red alga, Porphyridium cruentum. J Biol Chem. 1977;252:6421–3.

    Article  CAS  PubMed  Google Scholar 

  41. Priya B, Premanandh J, Dhanalakshmi RT, Seethalakshmi T, Uma L, Prabaharan D, Subramanian G. Comparative analysis of cyanobacterial superoxide dismutases to discriminate canonical forms. BMC Genom. 2007;8:1–10.

    Article  Google Scholar 

  42. Ismaiel MM, El-Ayouty YM, Loewen PC, Piercey-Normore MD. Characterization of the iron-containing superoxide dismutase and its response to stress in cyanobacterium Spirulina (Arthrospira) platensis. J Appl Phycol. 2014;26:1649–58.

    Article  CAS  Google Scholar 

  43. Sannasimuthu A, Kumaresan V, Pasupuleti M, Paray BA, Al-Sadoon MK, Arockiaraj J. Radical scavenging property of a novel peptide derived from C-terminal SOD domain of superoxide dismutase enzyme in Arthrospira platensis. Algal Res. 2018;35:519–29.

    Article  Google Scholar 

  44. Parker MS, Mock T, Armbrust EV. Genomic insights into marine microalgae. Annu Rev Genet. 2008;42:619–45.

    Article  CAS  PubMed  Google Scholar 

  45. Blaby-Haas CE, Merchant SS. Comparative and functional algal genomics. Annu Rev Plant Biol. 2019;70:605–38.

    Article  CAS  PubMed  Google Scholar 

  46. Berg G, Rybakova D, Fischer D, Cernava T, Vergès M-CC, Charles T, Chen X, Cocolin L, Eversole K, Corral GH. Microbiome definition re-visited: old concepts and new challenges. Microbiome. 2020;8:1–22.

    Google Scholar 

  47. Hoek C, Mann D, Jahns HM, Jahns M. Algae: an introduction to phycology. Cambridge University Press; 1995.

    Google Scholar 

  48. Singh S, Singh P. Effect of CO2 concentration on algal growth: a review. Renew Sustain Energy Rev. 2014;38:172–9.

    Article  CAS  Google Scholar 

  49. Safi C, Zebib B, Merah O, Pontalier P-Y, Vaca-Garcia C. Morphology, composition, production, processing and applications of Chlorella vulgaris: a review. Renew Sustain Energy Rev. 2014;35:265–78.

    Article  Google Scholar 

  50. Chisti Y. Biodiesel from microalgae. Biotechnol Adv. 2007;25:294–306.

    Article  CAS  PubMed  Google Scholar 

  51. Cheng Y-L, Juang Y-C, Liao G-Y, Ho S-H, Yeh K-L, Chen C-Y, Chang J-S, Liu J-C, Lee D-J. Dispersed ozone flotation of Chlorella vulgaris. Biores Technol. 2010;101:9092–6.

    Article  CAS  Google Scholar 

  52. De-Bashan LE, Bashan Y, Moreno M, Lebsky VK, Bustillos JJ. 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. 2002;48:514–21.

    Article  CAS  PubMed  Google Scholar 

  53. Gonzalez LE, Bashan Y. 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. 2000;66:1527–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Becker EW. Micro-algae as a source of protein. Biotechnol Adv. 2007;25:207–10.

    Article  CAS  PubMed  Google Scholar 

  55. Kumudha A, Selvakumar S, Dilshad P, Vaidyanathan G, Thakur MS, Sarada R. Methylcobalamin—a form of vitamin B12 identified and characterised in Chlorella vulgaris. Food Chem. 2015;170:316–20.

    Article  CAS  PubMed  Google Scholar 

  56. Phang S-M, Chu W-L, Rabiei R. Phycoremediation The algae world. Berlin: Springer; 2015. p. 357–89.

    Book  Google Scholar 

  57. Liu J, Danneels B, Vanormelingen P, Vyverman W. Nutrient removal from horticultural wastewater by benthic filamentous algae Klebsormidium sp., Stigeoclonium spp. and their communities: from laboratory flask to outdoor Algal Turf Scrubber (ATS). Water Res. 2016;92:61–8.

    Article  CAS  PubMed  Google Scholar 

  58. Teoh M-L, Chu W-L, Marchant H, Phang S-M. Influence of culture temperature on the growth, biochemical composition and fatty acid profiles of six Antarctic microalgae. J Appl Phycol. 2004;16:421–30.

    Article  CAS  Google Scholar 

  59. Oberholster PJ, Cheng P-H, Botha A-M, Genthe B. The potential of selected macroalgal species for treatment of AMD at different pH ranges in temperate regions. Water Res. 2014;60:82–92.

    Article  CAS  PubMed  Google Scholar 

  60. Takamura N, Kasai F, Watanabe MM. Effects of Cu, Cd and Zn on photosynthesis of freshwater benthic algae. J Appl Phycol. 1989;1:39–52.

    Article  CAS  Google Scholar 

  61. Stevens AE, McCarthy BC, Vis ML. Metal content of Klebsormidium-dominated (Chlorophyta) algal mats from acid mine drainage waters in southeastern Ohio. J Torrey Botan Soc. 2001;128:226–33.

    Article  Google Scholar 

  62. Luís AT, Durães N, de Almeida SFP, da Silva EF. Integrating geochemical (surface waters, stream sediments) and biological (diatoms) approaches to assess AMD environmental impact in a pyritic mining area: Aljustrel (Alentejo, Portugal). J Environ Sci. 2016;42:215–26.

    Article  CAS  Google Scholar 

  63. Valente T, Rivera M, Almeida S, Delgado C, Gomes P, Grande J, de La Torre M, Santisteban M. Characterization of water reservoirs affected by acid mine drainage: geochemical, mineralogical, and biological (diatoms) properties of the water. Environ Sci Pollut Res. 2016;23:6002–11.

    Article  CAS  Google Scholar 

  64. Freitas APP, Schneider IAH, Schwartzbold A. Biosorption of heavy metals by algal communities in water streams affected by the acid mine drainage in the coal-mining region of Santa Catarina state, Brazil. Miner Eng. 2011;24:1215–8.

    Article  CAS  Google Scholar 

  65. Sabater S, Buchaca T, Cambra J, Catalan J, Guasch H, Ivorra N, Muñoz I, Navarro E, Real M, Romaní A. Structure and function of benthic algal communities in an extremely acid river 1. J Phycol. 2003;39:481–9.

    Article  CAS  Google Scholar 

  66. Khan MI, Shin JH, Kim JD. The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Fact. 2018;17:1–21.

    Article  Google Scholar 

  67. Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G. Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv. 2014;32:1476–93.

    Article  CAS  PubMed  Google Scholar 

  68. Moriyama T, Toyoshima M, Saito M, Wada H, Sato N. Revisiting the algal “chloroplast lipid droplet”: the absence of an entity that is unlikely to exist. Plant Physiol. 2018;176:1519–30.

    Article  CAS  PubMed  Google Scholar 

  69. Fukuda H, Kondo A, Noda H. Biodiesel fuel production by transesterification of oils. J Biosci Bioeng. 2001;92:405–16.

    Article  CAS  PubMed  Google Scholar 

  70. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH. Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol. 2017;29:949–82.

    Article  CAS  PubMed  Google Scholar 

  71. Caporgno MP, Mathys A. Trends in microalgae incorporation into innovative food products with potential health benefits. Front Nutr. 2018;5:58.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J. TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol. 2012;23:352–63.

    Article  CAS  PubMed  Google Scholar 

  73. Xu Y, Caldo KMP, Pal-Nath D, Ozga J, Lemieux MJ, Weselake RJ, Chen G. Properties and biotechnological applications of acyl-CoA: diacylglycerol acyltransferase and phospholipid: diacylglycerol acyltransferase from terrestrial plants and microalgae. Lipids. 2018;53:663–88.

    Article  CAS  PubMed  Google Scholar 

  74. Lung S-C, Weselake RJ. Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids. 2006;41:1073–88.

    Article  CAS  PubMed  Google Scholar 

  75. Guo X, Fan C, Chen Y, Wang J, Yin W, Wang RR, Hu Z. Identification and characterization of an efficient acyl-CoA: diacylglycerol acyltransferase 1 (DGAT1) gene from the microalga Chlorella ellipsoidea. BMC Plant Biol. 2017;17:1–16.

    Article  CAS  Google Scholar 

  76. Wei H, Shi Y, Ma X, Pan Y, Hu H, Li Y, Luo M, Gerken H, Liu J. A type-I diacylglycerol acyltransferase modulates triacylglycerol biosynthesis and fatty acid composition in the oleaginous microalga, Nannochloropsis oceanica. Biotechnol Biofuels. 2017;10:1–18.

    Article  CAS  Google Scholar 

  77. Wagner M, Hoppe K, Czabany T, Heilmann M, Daum G, Feussner I, Fulda M. Identification and characterization of an acyl-CoA: diacylglycerol acyltransferase 2 (DGAT2) gene from the microalga O. tauri. Plant Physiol Biochem. 2010;48:407–16.

    Article  CAS  PubMed  Google Scholar 

  78. Niu Y-F, Zhang M-H, Li D-W, Yang W-D, Liu J-S, Bai W-B, Li H-Y. Improvement of neutral lipid and polyunsaturated fatty acid biosynthesis by overexpressing a type 2 diacylglycerol acyltransferase in marine diatom Phaeodactylum tricornutum. Mar Drugs. 2013;11:4558–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Manandhar-Shrestha K, Hildebrand M. Characterization and manipulation of a DGAT2 from the diatom Thalassiosira pseudonana: improved TAG accumulation without detriment to growth, and implications for chloroplast TAG accumulation. Algal Res. 2015;12:239–48.

    Article  Google Scholar 

  80. Klaitong P, Fa-Aroonsawat S, Chungjatupornchai W. Accelerated triacylglycerol production and altered fatty acid composition in oleaginous microalga Neochloris oleoabundans by overexpression of diacylglycerol acyltransferase 2. Microb Cell Fact. 2017;16:1–10.

    Article  CAS  Google Scholar 

  81. Li D-W, Cen S-Y, Liu Y-H, Balamurugan S, Zheng X-Y, Alimujiang A, Yang W-D, Liu J-S, Li H-Y. A type 2 diacylglycerol acyltransferase accelerates the triacylglycerol biosynthesis in heterokont oleaginous microalga Nannochloropsis oceanica. J Biotechnol. 2016;229:65–71.

    Article  CAS  PubMed  Google Scholar 

  82. Xin Y, Lu Y, Lee Y-Y, Wei L, Jia J, Wang Q, Wang D, Bai F, Hu H, Hu Q. Producing designer oils in industrial microalgae by rational modulation of co-evolving type-2 diacylglycerol acyltransferases. Mol Plant. 2017;10:1523–39.

    Article  CAS  PubMed  Google Scholar 

  83. Deng X-D, Gu B, Li Y-J, Hu X-W, Guo J-C, Fei X-W. The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii. Mol Plant. 2012;5:945–7.

    Article  CAS  PubMed  Google Scholar 

  84. La Russa M, Bogen C, Uhmeyer A, Doebbe A, Filippone E, Kruse O, Mussgnug JH. Functional analysis of three type-2 DGAT homologue genes for triacylglycerol production in the green microalga Chlamydomonas reinhardtii. J Biotechnol. 2012;162:13–20.

    Article  PubMed  CAS  Google Scholar 

  85. Cui Y, Zhao J, Wang Y, Qin S, Lu Y. Characterization and engineering of a dual-function diacylglycerol acyltransferase in the oleaginous marine diatom Phaeodactylum tricornutum. Biotechnol Biofuels. 2018;11:1–13.

    Article  CAS  Google Scholar 

  86. Xue J, Balamurugan S, Li D-W, Liu Y-H, Zeng H, Wang L, Yang W-D, Liu J-S, Li H-Y. Glucose-6-phosphate dehydrogenase as a target for highly efficient fatty acid biosynthesis in microalgae by enhancing NADPH supply. Metab Eng. 2017;41:212–21.

    Article  CAS  PubMed  Google Scholar 

  87. Zhu B-H, Tu C-C, Shi H-P, Yang G-P, Pan K-H. Overexpression of endogenous delta-6 fatty acid desaturase gene enhances eicosapentaenoic acid accumulation in Phaeodactylum tricornutum. Process Biochem. 2017;57:43–9.

    Article  CAS  Google Scholar 

  88. Fukuda S, Hirasawa E, Takemura T, Takahashi S, Chokshi K, Pancha I, Tanaka K, Imamura S. Accelerated triacylglycerol production without growth inhibition by overexpression of a glycerol-3-phosphate acyltransferase in the unicellular red alga Cyanidioschyzon merolae. Sci Rep. 2018;8:1–12.

    Article  Google Scholar 

  89. Rengel R, Smith RT, Haslam RP, Sayanova O, Vila M, Leon R. Overexpression of acetyl-CoA synthetase (ACS) enhances the biosynthesis of neutral lipids and starch in the green microalga Chlamydomonas reinhardtii. Algal Res. 2018;31:183–93.

    Article  Google Scholar 

  90. Osada K, Maeda Y, Yoshino T, Nojima D, Bowler C, Tanaka T. Enhanced NADPH production in the pentose phosphate pathway accelerates lipid accumulation in the oleaginous diatom Fistulifera solaris. Algal Res. 2017;23:126–34.

    Article  Google Scholar 

  91. Los DA, Murata N. Structure and expression of fatty acid desaturases. BBA Lipids Lipid Metabol. 1998;1394:3–15.

    Article  CAS  Google Scholar 

  92. de Jaeger L, Springer J, Wolbert EJ, Martens DE, Eggink G, Wijffels RH. Gene silencing of stearoyl-ACP desaturase enhances the stearic acid content in Chlamydomonas reinhardtii. Biores Technol. 2017;245:1616–26.

    Article  CAS  Google Scholar 

  93. Daboussi F, Leduc S, Marechal A, Dubois G, Guyot V, Perez-Michaut C, Amato A, Falciatore A, Juillerat A, Beurdeley M. Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun. 2014;5:1–7.

    Article  CAS  Google Scholar 

  94. Sorigué D, Légeret B, Cuiné S, Blangy S, Moulin S, Billon E, Richaud P, Brugière S, Couté Y, Nurizzo D. An algal photoenzyme converts fatty acids to hydrocarbons. Science. 2017;357:903–7.

    Article  PubMed  CAS  Google Scholar 

  95. Misra N, Panda PK, Parida BK, Mishra BK. dEMBF: a comprehensive database of enzymes of microalgal biofuel feedstock. PLoS ONE. 2016;11:e0146158.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Villarejo A, Orus MI, Martinez F. Regulation of the CO2-concentrating mechanism in Chlorella vulgaris UAM 101 by glucose. Physiol Plant. 1997;99:293–301.

    Article  CAS  Google Scholar 

  97. Fujiwara S, Fukuzawa H, Tachiki A, Miyachi S. Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci. 1990;87:9779–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G. A novel α-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J. 1998;17:1208–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Eriksson M, Karlsson J, Ramazanov Z, Gardeström P, Samuelsson G. Discovery of an algal mitochondrial carbonic anhydrase: molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii. Proc Natl Acad Sci. 1996;93:12031–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Geraghty AM, Spalding MH. Molecular and structural changes in Chlamydomonas under limiting CO2 (a possible mitochondrial role in adaptation). Plant Physiol. 1996;111:1339–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Moroney JV, Husic HD, Tolbert N. Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol. 1985;79:177–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Funke RP, Kovar JL, Weeks DP. Intracellular carbonic anhydrase is essential to photosynthesis in Chlamydomonas reinhardtii at atmospheric levels of CO2 (demonstration via genomic complementation of the high-CO2-requiring mutant ca-1). Plant Physiol. 1997;114:237–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Pronina NA, Semenenko VE. Membrane-bound carbonic anhydrase takes part in CO2 concentration in algae cells, Current research in photosynthesis. Berlin: Springer; 1990. p. 3283–6.

    Google Scholar 

  104. Pronina N, Borodin V. CO2 stress and CO2 concentration mechanism: investigation by means of photosystem-deficient and carbonic anhydrase-deficient mutants of Chlamydomonas reinhardtii. Photosynth Praha. 1993;28:515–515.

    CAS  Google Scholar 

  105. Raven JA. Photosynthetic and non-photosynthetic roles of carbonic anhydrase in algae and cyanobacteria. Phycologia. 1995;34:93–101.

    Article  Google Scholar 

  106. Park Y-I, Karlsson J, Rojdestvenski I, Pronina N, Klimov V, Öquist G, Samuelsson G. Role of a novel photosystem II-associated carbonic anhydrase in photosynthetic carbon assimilation in Chlamydomonas reinhardtii. FEBS Lett. 1999;444:102–5.

    Article  CAS  PubMed  Google Scholar 

  107. Eriksson M, Villand P, Gardeström P, Gr S. Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol. 1998;116:637–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Jo BH, Kang DG, Kim CS, Choi YS, Cha HJ. Biomineralization-based conversion of carbon dioxide to calcium carbonate using recombinant carbonic anhydrase. Chemosphere. 2012;87:1091–6.

    Article  PubMed  CAS  Google Scholar 

  109. Supuran CT, Vullo D, Manole G, Casini A, Scozzafava A. Designing of novel carbonic anhydrase inhibitors and activators. Curr Med Chem Cardiovasc Hematol Agents. 2004;2:49–68.

    Article  CAS  PubMed  Google Scholar 

  110. Kuo W-H, Yang S-F, Hsieh Y-S, Tsai C-S, Hwang W-L, Chu S-C. Differential expression of carbonic anhydrase isoenzymes in various types of anemia. Clin Chim Acta. 2005;351:79–86.

    Article  CAS  PubMed  Google Scholar 

  111. Borthwick K, Kandemir N, Topaloglu R, Kornak U, Bakkaloglu A, Yordam N, Ozen S, et al. A phenocopy of CAII deficiency: a novel genetic explanation for inherited infantile osteopetrosis with distal renal tubular acidosis. J Med Genet. 2003;40:115–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Parkkila S, Lasota J, Fletcher JA, Ou W-b, Kivelä AJ, Nuorva K, Parkkila A-K, Ollikainen J, Sly WS, Waheed A. Carbonic anhydrase II. A novel biomarker for gastrointestinal stromal tumors. Mod Pathol. 2010;23:743–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Service RF. Algae’s second try. Am Assoc Adv Sci. 2011;333:1238.

    Google Scholar 

  114. Bloch MR, Sasson J, Ginzburg ME, Goldman Z, Ginzburg BZ, Garti N, Porath A (1982) Oil products from algae. Google Patents

  115. Cannon GC, Heinhorst S, Kerfeld CA. Carboxysomal carbonic anhydrases: structure and role in microbial CO2 fixation. BBA Proteins. 2010;804:382–92.

    Article  CAS  Google Scholar 

  116. Pires J, Alvim-Ferraz M, Martins F, Simões M. Carbon dioxide capture from flue gases using microalgae: engineering aspects and biorefinery concept. Renew Sustain Energy Rev. 2012;16:3043–53.

    Article  CAS  Google Scholar 

  117. González-Fernández C, Ballesteros M. Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation. Biotechnol Adv. 2012;30:1655–61.

    Article  PubMed  CAS  Google Scholar 

  118. Shekh AY, Krishnamurthi K, Mudliar SN, Yadav RR, Fulke AB, Devi SS, Chakrabarti T. Recent advancements in carbonic anhydrase–driven processes for CO2 sequestration: minireview. Crit Rev Environ Sci Technol. 2012;42:1419–40.

    Article  CAS  Google Scholar 

  119. Ramanan R, Kannan K, Deshkar A, Yadav R, Chakrabarti T. Enhanced algal CO2 sequestration through calcite deposition by Chlorella sp. and Spirulina platensis in a mini-raceway pond. Biores Technol. 2010;101:2616–22.

    Article  CAS  Google Scholar 

  120. Fulke AB, Mudliar S, Yadav R, Shekh A, Srinivasan N, Ramanan R, Krishnamurthi K, Devi SS, Chakrabarti T. Bio-mitigation of CO2, calcite formation and simultaneous biodiesel precursors production using Chlorella sp. Biores Technol. 2010;101:8473–6.

    Article  CAS  Google Scholar 

  121. Fisher SZ, Aggarwal M, Kovalevsky AY, Silverman DN, McKenna R. Neutron diffraction of acetazolamide-bound human carbonic anhydrase II reveals atomic details of drug binding. J Am Chem Soc. 2012;134:14726–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Vignais PM, Billoud B, Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol Rev. 2001;25:455–501.

    Article  CAS  PubMed  Google Scholar 

  123. Gutekunst K, Hoffmann D, Lommer M, Egert M, Suzuki I, Schulz-Friedrich R, Appel J. Metal dependence and intracellular regulation of the bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803. Int J Hydrogen Energy. 2006;31:1452–9.

    Article  CAS  Google Scholar 

  124. Dutta D, De D, Chaudhuri S, Bhattacharya SK. Hydrogen production by cyanobacteria. Microb Cell Fact. 2005;4:1–11.

    Article  CAS  Google Scholar 

  125. Gil JM, Gil FM (2004) Complejos precursores para la generación de hidrógeno y oxigeno en procesos miméticos de la fotosíntesis. Premio de Investigación Caja España

  126. Contreras Pérez JB, Scott JA, Mendoza Gómez CL, Espinal G, Zapata Z (2008) Potencial de algas verdes para la producción fotobiológica de hidrógeno. Ciencia y sociedad

  127. Dunn S. Hydrogen futures: toward a sustainable energy system. Int J Hydrogen energy. 2002;27:235–64.

    Article  CAS  Google Scholar 

  128. Brandon N, Kurban Z. Clean energy and the hydrogen economy. Philos Trans R Soc A Math Phys Eng Sci. 2017;375:20160400.

    Article  CAS  Google Scholar 

  129. Service RF. The hydrogen backlash. Am Assoc Adv Sci 2004;305:958-961

    CAS  Google Scholar 

  130. Preuster P, Alekseev A, Wasserscheid P. Hydrogen storage technologies for future energy systems. Annu Rev Chem Biomol Eng. 2017;8:445–71.

    Article  CAS  PubMed  Google Scholar 

  131. Mohanan N, Satyanarayana T Amylases. In: Schmidt TM, ediotor. Encyclopedia of microbiology. Elsevier. 2019. p. 107–126. https://doi.org/10.1016/B978-0-12-809633-8.13003-1

  132. Frantz SC, Paludo LC, Stutz H, Spier MR. Production of amylases from Coprinus comatus under submerged culture using wheat-milling by-products: optimization, kinetic parameters, partial purification and characterization. Biocatal Agric Biotechnol. 2019;17:82–92.

    Article  Google Scholar 

  133. Simair AA, Qureshi AS, Khushk I, Ali CH, Lashari S, Bhutto MA, Mangrio GS, Lu C. Production and partial characterization of α-amylase enzyme from Bacillus sp. BCC 01-50 and potential applications. BioMed Res Int. 2017;2017:9173040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  134. Paludo LC, Frantz SC, Ançay R Jr, Stutz H, Dantas TLP, Spier MR. Optimization, kinetic and bioprocess parameters of amylases production from Coprinus comatus under submerged culture using starch-based simple medium: partial enzyme characterization. Biocatal Agric Biotechnol. 2018;16:529–37.

    Article  Google Scholar 

  135. Souza PMd, Magalhães PdO. Application of microbial α-amylase in industry—a review. Braz J Microbiol. 2010;41:850–61.

    Article  PubMed  PubMed Central  Google Scholar 

  136. Zhang Q, Han Y, Xiao H. Microbial α-amylase: a biomolecular overview. Process Biochem. 2017;53:88–101.

    Article  CAS  Google Scholar 

  137. Fogarty WM, Kelly CT. Recent advances in microbial amylases. In: Fogarty WM, Kelly CT (eds) Microbial enzymes and biotechnology. Dordrecht: Springer; 1990. https://doi.org/10.1007/978-94-009-0765-2_3

  138. Shigemura M, Moriyama T, Endo T, Shibuya H, Suzuki H, Nishimura M, Chiba H, Matsuno K. Myeloma cells produce sialyl salivary-type amylase. CCLM. 2004;42:677–80.

    Article  CAS  PubMed  Google Scholar 

  139. Abou-Seif MA, Youssef A-A. Evaluation of some biochemical changes in diabetic patients. Clin Chim Acta. 2004;346:161–70.

    Article  CAS  PubMed  Google Scholar 

  140. Lin LL, Chyau CC, Hsu WH. Production and properties of a raw-starch-degrading amylase from the thermophilic and alkaliphilic Bacillus sp. TS-23. Biotechnol Appl Biochem. 1998;28:61–8.

    CAS  PubMed  Google Scholar 

  141. Lin LL, Hsu WH, Chu WS. A gene encoding for an α-amylase from thermophilic Bacillus sp. strain TS-23 and its expression in Escherichia coli. J Appl Microbiol. 1997;82:325–34.

    Article  CAS  PubMed  Google Scholar 

  142. Pandey A, Soccol CR, Mitchell D. New developments in solid state fermentation: I-bioprocesses and products. Process Biochem. 2000;35:1153–69.

    Article  CAS  Google Scholar 

  143. Regalado C, García-Almendárez BE, Duarte-Vázquez MA. Biotechnological applications of peroxidases. Phytochem Rev. 2004;3:243–56.

    Article  CAS  Google Scholar 

  144. Dhruvaraj M. Role of peroxidase in clinical assays: a short review. J Clin Nutr. 2017;3:14.

    Google Scholar 

  145. Bansal N, Kanwar SS. Peroxidase (s) in environment protection. Sci World J. 2013;2013:1.

    Article  CAS  Google Scholar 

  146. Huber P, Carré B. Decolorization of process waters in deinking mills and similar applications: a review. BioResources. 2012;7:1366–82.

    Google Scholar 

  147. Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T. New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol. 2010;87:871–97.

    Article  CAS  PubMed  Google Scholar 

  148. Marco-Urrea E, Reddy C. Degradation of chloro-organic pollutants by white rot fungi, Microbial degradation of xenobiotics. Berlin: Springer; 2012. p. 31–66.

    Book  Google Scholar 

  149. Parkin KL. Fennema’s food chemistry. CRC; 2017.

    Google Scholar 

  150. Kaiser M, Huber R, Ehrmann M. Proteases. In: Pentimalli F, Giordano A, editors. Reference module in life sciences. Oxford: Elsevier; 2017.

    Google Scholar 

  151. dos Santos Aguilar JG, Sato HH. Microbial proteases: production and application in obtaining protein hydrolysates. Food Res Int. 2018;103:253–62.

    Article  PubMed  CAS  Google Scholar 

  152. Savitha S, Sadhasivam S, Swaminathan K, Lin FH. Fungal protease: production, purification and compatibility with laundry detergents and their wash performance. J Taiwan Inst Chem Eng. 2011;42:298–304.

    Article  CAS  Google Scholar 

  153. Abidi F, Chobert J-M, Haertlé T, Marzouki MN. Purification and biochemical characterization of stable alkaline protease Prot-2 from Botrytis cinerea. Process Biochem. 2011;46:2301–10.

    Article  CAS  Google Scholar 

  154. Gupta R, Beg Q, Lorenz P. Bacterial alkaline proteases: molecular approaches and industrial applications. Appl Microbiol Biotechnol. 2002;59:15–32.

    Article  CAS  PubMed  Google Scholar 

  155. Johnvesly B, Naik G. Studies on production of thermostable alkaline protease from thermophilic and alkaliphilic Bacillus sp. JB-99 in a chemically defined medium. Process Biochem. 2001;37:139–44.

    Article  CAS  Google Scholar 

  156. Li Q, Yi L, Marek P, Iverson BL. Commercial proteases: present and future. FEBS Lett. 2013;587:1155–63.

    Article  CAS  PubMed  Google Scholar 

  157. Rao YK, Lu S-C, Liu B-L, Tzeng Y-M. Enhanced production of an extracellular protease from Beauveria bassiana by optimization of cultivation processes. Biochem Eng J. 2006;28:57–66.

    Article  CAS  Google Scholar 

  158. Hajji M, Hmidet N, Jellouli K, Vallaeys T, Nasri M, Sellami-Kamoun A. Gene cloning and expression of a detergent stable alkaline protease from Aspergillus clavatus ES1. Process Biochem. 2010;45:1746–52.

    Article  CAS  Google Scholar 

  159. Tavano OL. Protein hydrolysis using proteases: an important tool for food biotechnology. J Mol Catal B Enzym. 2013;90:1–11.

    Article  CAS  Google Scholar 

  160. Tomar R, Kumar R, Jagannadham M. A stable serine protease, wrightin, from the latex of the plant Wrightia tinctoria (Roxb.) R. Br.: purification and biochemical properties. J Agric Food Chem. 2008;56:1479–87.

    Article  CAS  PubMed  Google Scholar 

  161. Hasan F, Shah AA, Hameed A. Industrial applications of microbial lipases. Enzyme Microb Technol. 2006;39:235–51.

    Article  CAS  Google Scholar 

  162. Andualema B, Gessesse A. Microbial lipases and their industrial applications. Biotechnology. 2012;11:100.

    Article  CAS  Google Scholar 

  163. Fendri I, Chaari A, Dhouib A, Jlassi B, Abousalham A, Carrière F, Sayadi S, Abdelkafi S. Isolation, identification and characterization of a new lipolytic Pseudomonas sp., strain AHD-1, from Tunisian soil. Environ Technol. 2010;31:87–95.

    Article  CAS  PubMed  Google Scholar 

  164. Barouh N, Abdelkafi S, Fouquet B, Pina M, Scheirlinckx F, Carrière F, Villeneuve P. Neutral lipid characterization of non-water-soluble fractions of carica papaya latex. J Am Oil Chem Soc. 2010;87:987–95.

    Article  CAS  Google Scholar 

  165. Khannous L, Jrad M, Dammak M, Miladi R, Chaaben N, Khemakhem B, Gharsallah N, Fendri I. Isolation of a novel amylase and lipase-producing Pseudomonas luteola strain: study of amylase production conditions. Lipids Health Dis. 2014;13:1–9.

    Article  CAS  Google Scholar 

  166. Guerrand D. Lipases industrial applications: focus on food and agroindustries. OCL Oilseeds Fats Crops Lipids. 2017;24:D403.

    Google Scholar 

  167. Dutra JC, da Terzi SC, Bevilaqua JV, Damaso MC, Couri S, Langone MA, Senna LF. Lipase production in solid-state fermentation monitoring biomass growth of Aspergillus niger using digital image processing, biotechnology for fuels and chemicals. Berlin: Springer; 2007. p. 431–43.

    Google Scholar 

  168. Griebeler N, Polloni AE, Remonatto D, Arbter F, Vardanega R, Cechet JL, Di Luccio M, de Oliveira D, Treichel H, Cansian RL. Isolation and screening of lipase-producing fungi with hydrolytic activity. Food Bioprocess Technol. 2011;4:578–86.

    Article  CAS  Google Scholar 

  169. Abada EAE. Production and characterization of a mesophilic lipase isolated from Bacillus stearothermophilus AB-1. Pak J Biol Sci. 2008;11:1100–6.

    Article  PubMed  Google Scholar 

  170. Treichel H, de Oliveira D, Mazutti MA, Di Luccio M, Oliveira JV. A review on microbial lipases production. Food Bioprocess Technol. 2010;3:182–96.

    Article  CAS  Google Scholar 

  171. Gross R, Kalra B, Kumar A. Polyester and polycarbonate synthesis by in vitro enzyme catalysis. Appl Microbiol Biotechnol. 2001;55:655–60.

    Article  CAS  PubMed  Google Scholar 

  172. Kim DY, Dordick JS. Combinatorial array-based enzymatic polyester synthesis. Biotechnol Bioeng. 2001;76:200–6.

    Article  CAS  PubMed  Google Scholar 

  173. Singh A, Nigam PS, Murphy JD. Renewable fuels from algae: an answer to debatable land based fuels. Biores Technol. 2011;102:10–6.

    Article  CAS  Google Scholar 

  174. Wang K, Brown RC, Homsy S, Martinez L, Sidhu SS. Fast pyrolysis of microalgae remnants in a fluidized bed reactor for bio-oil and biochar production. Biores Technol. 2013;127:494–9.

    Article  CAS  Google Scholar 

  175. Patel RN. Enzymatic synthesis of chiral intermediates for drug development. Adv Synth Catal. 2001;343:527–46.

    Article  CAS  Google Scholar 

  176. Liese A, Seelbach K, Wandrey C. Industrial biotransformations. Wiley; 2006.

    Book  Google Scholar 

  177. Tanaka K, Yoshida K, Sasaki C, Osano YT. Practical asymmetric synthesis of the herbicide (S)-indanofan via lipase-catalyzed kinetic resolution of a diol and stereoselective acid-catalyzed hydrolysis of a chiral epoxide. J Org Chem. 2002;67:3131–3.

    Article  CAS  PubMed  Google Scholar 

  178. Song H-Y, El Sheikha AF, Hu D-M. The positive impacts of microbial phytase on its nutritional applications. Trends Food Sci Technol. 2019;86:553–62.

    Article  CAS  Google Scholar 

  179. Spier MR, Rodrigues M, Paludo L, Cerutti ML. Perspectives of phytases in nutrition, biocatalysis, and soil stabilization, enzymes in human and animal nutrition. Oxford: Elsevier; 2018. p. 89–104.

    Book  Google Scholar 

  180. Spier MR, Behsnilian D, Zielinski A, Konietzny U, Greiner R. Studies towards the stabilisation of a mushroom phytase produced by submerged cultivation. Protein J. 2015;34:367–79.

    Article  CAS  PubMed  Google Scholar 

  181. Vasudevan UM, Jaiswal AK, Krishna S, Pandey A. Thermostable phytase in feed and fuel industries. Biores Technol. 2019;278:400–7.

    Article  CAS  Google Scholar 

  182. Haefner S, Knietsch A, Scholten E, Braun J, Lohscheidt M, Zelder O. Biotechnological production and applications of phytases. Appl Microbiol Biotechnol. 2005;68:588–97.

    Article  CAS  PubMed  Google Scholar 

  183. Vohra A, Satyanarayana T. Phytases: microbial sources, production, purification, and potential biotechnological applications. Crit Rev Biotechnol. 2003;23:29–60.

    Article  CAS  PubMed  Google Scholar 

  184. Singh B, Satyanarayana T. Microbial phytases in phosphorus acquisition and plant growth promotion. Physiol Mol Biol Plants. 2011;17:93–103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Turner BL, Mahieu N, Condron LM. Quantification of myo-inositol hexakisphosphate in alkaline soil extracts by solution 31P NMR spectroscopy and spectral deconvolution. Soil Sci. 2003;168:469–78.

    Article  CAS  Google Scholar 

  186. Mullen MD. Phosphorus in soils: biological interactions. In: Hillel D, editor. Encyclopedia of soils in the environment. Oxford: Elsevier; 2005. p. 210–215

  187. Richardson AE, Hadobas PA, Hayes JE. Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J. 2001;25:641–9.

    Article  CAS  PubMed  Google Scholar 

  188. Hayes JE, Richardson AE, Simpson RJ. Phytase and acid phosphatase activities in extracts from roots of temperate pasture grass and legume seedlings. Funct Plant Biol. 1999;26:801–9.

    Article  CAS  Google Scholar 

  189. Yoon SJ, Choi YJ, Min HK, Cho KK, Kim JW, Lee SC, Jung YH. Isolation and identification of phytase-producing bacterium, Enterobacter sp. 4, and enzymatic properties of phytase enzyme. Enzyme Microb Technol. 1996;18:449–54.

    Article  CAS  Google Scholar 

  190. Jorquera M, Martínez O, Maruyama F, Marschner P, de la Luz MM. Current and future biotechnological applications of bacterial phytases and phytase-producing bacteria. Microbes Environ. 2008;23:182–91.

    Article  PubMed  Google Scholar 

  191. Hariprasad P, Niranjana S. Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant Soil. 2009;316:13–24.

    Article  CAS  Google Scholar 

  192. Patel KJ, Singh AK, Nareshkumar G, Archana G. Organic-acid-producing, phytate-mineralizing rhizobacteria and their effect on growth of pigeon pea (Cajanus cajan). Appl Soil Ecol. 2010;44:252–61.

    Article  Google Scholar 

  193. Kumar V, Singh P, Jorquera MA, Sangwan P, Kumar P, Verma A, Agrawal S. Isolation of phytase-producing bacteria from Himalayan soils and their effect on growth and phosphorus uptake of Indian mustard (Brassica juncea). World J Microbiol Biotechnol. 2013;29:1361–9.

    Article  CAS  PubMed  Google Scholar 

  194. Singh P, Kumar V, Agrawal S. Evaluation of phytase producing bacteria for their plant growth promoting activities. Int J Microbiol. 2014;2014:1.

    Google Scholar 

  195. Luís AT, Teixeira P, Almeida SFP, Matos JX, da Silva EF. Environmental impact of mining activities in the Lousal area (Portugal): chemical and diatom characterization of metal-contaminated stream sediments and surface water of Corona stream. Sci Total Environ. 2011;409:4312–25.

    Article  PubMed  CAS  Google Scholar 

  196. de Jesus Raposo MF, de Morais RMSC, de Morais AMMB. Health applications of bioactive compounds from marine microalgae. Life Sci. 2013;93:479–86.

    Article  PubMed  CAS  Google Scholar 

  197. Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem. 1995;64:97–112.

    Article  CAS  PubMed  Google Scholar 

  198. Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG. The role and evolution of superoxide dismutases in algae 1. J Phycol. 2005;41:453–65.

    Article  CAS  Google Scholar 

  199. Herbert SK, Samson G, Fork DC, Laudenbach DE. Characterization of damage to photosystems I and II in a cyanobacterium lacking detectable iron superoxide dismutase activity. Proc Natl Acad Sci. 1992;89:8716–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Maté D, García-Ruiz E, Camarero S, Alcalde M. Directed evolution of fungal laccases. Curr Genom. 2011;12:113–22.

    Article  Google Scholar 

  201. Lisov A, Zavarzina A, Zavarzin A, Demin V, Leontievsky A. Dimeric and monomeric laccases of soil-stabilizing lichen Solorina crocea: purification, properties and reactions with humic acids. Soil Biol Biochem. 2012;45:161–7.

    Article  CAS  Google Scholar 

  202. Baldrian P. Fungal laccases—occurrence and properties. FEMS Microbiol Rev. 2006;30:215–42.

    Article  CAS  PubMed  Google Scholar 

  203. Giardina P, Sannia G. Laccases: old enzymes with a promising future. Cell Mol Life Sci. 2015;72:855–6.

    Article  CAS  PubMed  Google Scholar 

  204. Piscitelli A, Del Vecchio C, Faraco V, Giardina P, Macellaro G, Miele A, Pezzella C, Sannia G. Fungal laccases: versatile tools for lignocellulose transformation. CR Biol. 2011;334:789–94.

    Article  CAS  Google Scholar 

  205. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL. Towards environmental systems biology of Shewanella. Nat Rev Microbiol. 2008;6:592–603.

    Article  CAS  PubMed  Google Scholar 

  206. Nealson KH, Belz A, McKee B. Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek. 2002;81:215–22.

    Article  CAS  PubMed  Google Scholar 

  207. Shi L, Rosso KM, Clarke TA, Richardson DJ, Zachara JM, Fredrickson JK. Molecular underpinnings of Fe (III) oxide reduction by Shewanella oneidensis MR-1. Front Microbiol. 2012;3:50.

    Article  PubMed  PubMed Central  Google Scholar 

  208. Acuner E, Dilek F. Treatment of tectilon yellow 2G by Chlorella vulgaris. Process Biochem. 2004;39:623–31.

    Article  CAS  Google Scholar 

  209. Daneshvar N, Ayazloo M, Khataee A, Pourhassan M. Biological decolorization of dye solution containing Malachite Green by microalgae Cosmarium sp. Biores Technol. 2007;98:1176–82.

    Article  CAS  Google Scholar 

  210. Otto B, Schlosser D. First laccase in green algae: purification and characterization of an extracellular phenol oxidase from Tetracystis aeria. Planta. 2014;240:1225–36.

    Article  CAS  PubMed  Google Scholar 

  211. Katrolia P, Rajashekhara E, Yan Q, Jiang Z. Biotechnological potential of microbial α-galactosidases. Crit Rev Biotechnol. 2014;34:307–17.

    Article  CAS  PubMed  Google Scholar 

  212. Weignerová L, Simerská P, Křen V. α-Galactosidases and their applications in biotransformations. Biocatal Biotransform. 2009;27:79–89.

    Article  CAS  Google Scholar 

  213. Linden JC. Immobilized α-d-galactosidase in the sugar beet industry. Enzyme Microb Technol. 1982;4:130–6.

    Article  CAS  Google Scholar 

  214. Alegra T, Vairo F, de Souza MV, Krug BC, Schwartz IV. Enzyme replacement therapy for Fabry disease: a systematic review and meta-analysis. Genet Mol Biol. 2012;35:947–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Pisani A, Visciano B, Roux GD, Sabbatini M, Porto C, Parenti G, Imbriaco M. Enzyme replacement therapy in patients with Fabry disease: state of the art and review of the literature. Mol Genet Metab. 2012;107:267–75.

    Article  CAS  PubMed  Google Scholar 

  216. Zeyland J, Gawrońska B, Juzwa W, Jura J, Nowak A, Słomski R, Smorąg Z, Szalata M, Woźniak A, Lipiński D. Transgenic pigs designed to express human α-galactosidase to avoid humoral xenograft rejection. J Appl Genet. 2013;54:293–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Choi S-Y, Jeong H-J, Lim H-G, Park S-S, Kim S-H, Kim YJ. Elimination of α-gal xenoreactive epitope: α-galactosidase treatment of porcine heart valves. J Heart Valve Dis. 2012;21:387.

    PubMed  Google Scholar 

  218. Sweeney MD, Xu F. Biomass converting enzymes as industrial biocatalysts for fuels and chemicals: recent developments. Catalysts. 2012;2:244–63.

    Article  CAS  Google Scholar 

  219. de Almeida MN, Guimarães VM, Bischoff KM, Falkoski DL, Pereira OL, Gonçalves DS, de Rezende ST. Cellulases and hemicellulases from endophytic Acremonium species and its application on sugarcane bagasse hydrolysis. Appl Biochem Biotechnol. 2011;165:594–610.

    Article  PubMed  CAS  Google Scholar 

  220. Husain Q. β Galactosidases and their potential applications: a review. Crit Rev Biotechnol. 2010;30:41–62.

    Article  CAS  PubMed  Google Scholar 

  221. Oliveira C, Guimarães PM, Domingues L. Recombinant microbial systems for improved β-galactosidase production and biotechnological applications. Biotechnol Adv. 2011;29:600–9.

    Article  CAS  PubMed  Google Scholar 

  222. Cachumba JJM, Antunes FAF, Peres GFD, Brumano LP, Santos JCD, Silva SSD. Current applications and different approaches for microbial l-asparaginase production. Braz J Microbiol. 2016;47:77–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Hosamani R, Kaliwal B. L-asparaginase an anti-tumor agent production by Fusarium equiseti using solid state fermentation. Int J Drug Discov. 2011;3:88–99.

    Article  Google Scholar 

  224. Salzer WL, Asselin BL, Plourde PV, Corn T, Hunger SP. Development of asparaginase Erwinia chrysanthemi for the treatment of acute lymphoblastic leukemia. Ann N Y Acad Sci. 2014;1329:81–92.

    Article  CAS  PubMed  Google Scholar 

  225. Sinha R, Singh H, Jha S. Microbial l-asparaginase: present and future prospective. Int J Innov Res Sci Eng. 2013;2:7031–51.

    Google Scholar 

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  1. Department of Biology, Islamic Azad University of Urmia, Urmia, Iran

    Mohammad Amin Shoarnaghavi & Arian Amirifar

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, 201303, India

    Arti Mishra

  3. Indira Gandhi Agricultural University, Raipur, Chhattisgarh, 492012, India

    Smruthi Sagarika Mahapatra

  4. 12/9 Browns Avenue, Ringwood, Melbourne, VIC, 3134, Australia

    Khatereh Nobaharan

  5. Department of Soil Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

    Arash Hemati & Behnam Asgari Lajayer

  6. Faculty of Agriculture, Dalhousie University, Truro, NS, B2N 5E3, Canada

    Tess Astatkie

Authors
  1. Mohammad Amin Shoarnaghavi
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  2. Arti Mishra
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  3. Arian Amirifar
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  4. Smruthi Sagarika Mahapatra
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  5. Khatereh Nobaharan
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  6. Arash Hemati
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  7. Behnam Asgari Lajayer
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  8. Tess Astatkie
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Contributions

MAS and AA: Wrote the first draft of the manuscript and all authors commented on previous versions of the manuscript. AM, SSM, KN, and AH: Helped with constructive discussions and revision of the manuscript. BAL and TA: Helped with constructive discussions, and revision and submission of the manuscript.

Corresponding authors

Correspondence to Behnam Asgari Lajayer or Tess Astatkie.

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Shoarnaghavi, M.A., Mishra, A., Amirifar, A. et al. Soil algae enzymes and their biotechnological applications. Syst Microbiol and Biomanuf 2, 589–606 (2022). https://doi.org/10.1007/s43393-022-00095-7

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  • DOI: https://doi.org/10.1007/s43393-022-00095-7

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