Unveiling the antioxidant capacity of fermented foods and food microorganisms: a focus on cyanobacteria

Agarwal P, Soni R, Kaur P, Madan A, Mishra R, Pandey J, Singh S, Singh G (2022) Cyanobacteria as a promising alternative for sustainable environment: synthesis of biofuel and biodegradable plastics. Front Microbiol 13:939347

Alghazwi M, Kan YQ, Zhang W, Gai WP, Garson MJ, Smid S (2016) Neuroprotective activities of natural products from marine macroalgae during 1999–2015. J Appl Phycol 28:3599–3616

Anantharajappa K, Dharmesh SM, Ravi S (2020) Gastro-protective potentials of spirulina: role of vitamin B12. J Food Sci Technol 57:745–753

Andrade MA, Lima V, Sanches-Silva A, Vilarinho F, Castilho MC, Khwaldia K, Ramos F (2019) Pomegranate and grape by-products and their active compounds: are they a valuable source for food applications? Trends Food Sci Technol 86:68–84

Bavini JM (2018) Cyanobacteria in skin protection. Master's Thesis, Faculdade de Ciências Universidade do Porto, Porto, Portugal. https://repositorio-aberto.up.pt/bitstream/10216/118610/2/311491

Belay A (2002) The potential application of spirulina [Arthrospira] as a nutritional and therapeutic supplement in health management. J Am Nutraceut Assoc 5:27–48

Böttger A, Vothknecht U, Bolle C, Wolf A (2018) Plant secondary metabolites and their general function in plants. In: Lessons on caffeine, Cannabis & Co. Springer, Cham, pp 3–17

Chomel M, Guittonny-Larchevêque M, Fernandez C, Gallet C, DesRochers A, Paré D, Jackson BG, Baldy V (2016) Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. J Ecol 104:1527–1541

Browne D, McGuinness B, Woodside JV, McKay GJ (2019) Vitamin E and Alzheimer’s disease: what do we know so far? Clin Interv Aging 14:1303–1317

Calder PC (2013) Omega-3 fatty acids and inflammatory processes. Nutrients 5:2014–2037

Chandra AS, Rajashekhar M (2013) Antioxidant activity in the four species of cyanobacteria isolated from a sulfur spring in the western Ghats of Karnataka. Int J Pharm Biol Sci 4:275–285

Challouf R, Trabelsi L, Ben Dhieb R, El Abed O, Yahia A, Ghozzi K, Ben Ammar J, Omran H, Ben Ouada H (2011) Evaluation of cytotoxicity and biological activities in extracellular polysaccharides released by cyanobacterium Arthrospira platensis. Braz Arch Biol Technol 54(4):831–838. https://doi.org/10.1590/S1516-89132011000400024

Chan M, Liu D, Wu Y, Yang F, Howell K (2021) Microorganisms in whole botanical fermented foods survive processing and simulated digestion to affect gut microbiota composition. Front Microbiol 12:759708. https://doi.org/10.3389/fmicb.2021.759708

Chen B, You W, Huang J et al (2010) Isolation and antioxidant property of the extracellular polysaccharide from Rhodella reticulata. World J Microbiol Biotechnol 26:833–840. https://doi.org/10.1007/s11274-009-0240-y

Chernane H, Mansori M, Latique S, El Kaoua M (2014) Evaluation of antioxidant capacity of methanol extract and its solvent fractions obtained from four Moroccan macro algae species. Eur Sci J 10:35–48

Chittapun S, Jonjaroen V, Khumrangsee K, Charoenrat T (2020) C-phycocyanin extraction from two freshwater cyanobacteria by freeze thaw and pulsed electric field techniques to improve extraction efficiency and purity. Algal Res 46:101789

Chittora D, Meena M, Barupal T, Swapnil P (2020) Cyanobacteria as a source of biofertilizers for sustainable agriculture. Biochem Biophys Rep 22:100737

Choi WY, Kang DH, Heo SJ, Lee HY (2018) Enhancement of the neuroprotective effect of fermented spirulina maxima associated with antioxidant activities by ultrasonic extraction. Appl Sci 8:2469

Cikoš AM, Jurin M, Čož-Rakovac R, Jokić S, Jerković I (2019) Update on monoterpenes from red macroalgae: isolation, analysis, and bioactivity. Mar Drugs 17:537

Colusse GA, Mendes CRB, Duarte MER, de Carvalho JC, Noseda MD (2020) Effects of different culture media on physiological features and laboratory scale production cost of Dunaliella salina. Biotechnol Rep 27:e00508. https://doi.org/10.1016/j.btre.2020.e00508

Derias MSM, Sabaa ARFA, Osman AEMA, Mohamed AEHA, Darwish DAABA (2021) The potential protective role of astaxanthin on doxorubicin-induced cardiac toxicity in rats. QJM Int J Med 114:117003

El-Aty AMA, Mohame AA, Samhan FA (2014) In vitro antioxidant and antibacterial activities of two fresh water cyanobacterial species, Oscillatoria agardhii and Anabaena sphaerica. J Appl Pharm Sci 4:69–75

Fais G, Manca A, Bolognesi F, Borselli M, Concas A, Busutti M, Broggi G, Sanna P, Castillo-Aleman YM, Rivero-Jiménez RA, Hernandez AAB, Carmenate YV, Altea M, Pantaleo A, Gabrielli G, Biglioli F, Cao G, Giannaccare G (2022) Wide range applications of spirulina: from earth to space missions. Mar Drugs 20:299

Fallas Rodríguez P, Murillo-González L, Rodríguez E, Pérez AM (2023) Marine phenolic compounds: sources, commercial value, and biological activities. In: Pérez-Correa JR, Mateos R, Domínguez H (eds) Marine phenolic compounds. Elsevier, Amsterdam, pp 47–86

Fields FJ, Lejzerowicz F, Schroeder D, Ngoi SM, Tran M, McDonald D, Jiang L, Chang JT, Knight R, Mayfield S (2020) Effects of the microalgae chlamydomonas on gastrointestinal health. J Funct Foods 65:103738

Gänzle MG (2014) Enzymatic and bacterial conversions during sourdough fermentation. Food Microbiol 37:2–10

Garofalo C, Norici A, Mollo L, Osimani A, Aquilanti L (2022) Fermentation of microalgal biomass for innovative food production. Microorganisms 10:2069

Geethu V, Shamina M (2018) Antioxidant activity of cyanobacterium Nostoc spongiaeforme C. Agardh ex Born. & Flah. J Algal Biomass Util 9:26–30

Gibson RS, Bailey KB, Gibbs M, Ferguson EL (2010) A review of phytate, iron, zinc, and calcium concentrations in plant-based complementary foods used in low-income countries and implications for bioavailability. Food Nutr Bull 31(2 Suppl.):S134–S146

Gouveia L, Raymundo A, Batista AP et al (2006) Chlorella vulgaris and Haematococcus pluvialis biomass as colouring and antioxidant in food emulsions. Eur Food Res Technol 222:362–367. https://doi.org/10.1007/s00217-005-0105-z

Gregoire E, Pirotte BF, Moerman F, Altdorfer A, Gaspard L, Firre E, Moonen M, Darcis G (2022) Mycobacterium avium complex and Cryptococcus neoformans co-infection in a patient with acquired immunodeficiency syndrome: a case report. Acta Clin Belg Int J Clin Lab Med 77:679–684

Guerreiro A, Andrade MA, Menezes C, Vilarinho F, Dias E (2020) Antioxidant and cytoprotective properties of cyanobacteria: potential for biotechnological applications. Toxins 12:548

Gupta S, Gupta C, Prakash D (2017) Prebiotic efficiency of blue green algae on probiotics microorganisms. J Microbiol Exp 4:120

Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

Hannan MA, Sohag AAM, Dash R, Haque MN, Mohibbullah M, Oktaviani DF, Hossain MT, Choi HJ, Moon IS (2020) Phytosterols of marine algae: insights into the potential health benefits and molecular pharmacology. Phytomedicine 69:153201

Hashtroudi MS, Shariatmadari Z, Riahi H, Ghassempour A (2013) Analysis of Anabaena vaginicola and Nostoc calcicola from Northern Iran, as rich sources of major carotenoids. Food Chem 136:1148–1153

Hayashi T, Hayashi K, Maeda M, Kojima I (1996) Calcium Spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis. J Nat Prod 59:83–87

Heaney RP (2000) Calcium, dairy products and osteoporosis. J Am Coll Nutr 19(2 Suppl.):83S-99S

Hirahashi T, Matsumoto M, Hazeki K, Saeki Y, Ui M, Seya T (2002) Activation of the human innate immune system by spirulina: augmentation of interferon production and NK cytotoxicity by oral administration of hot water extract of Spirulina platensis. Int Immuno Pharmacol 2:423–434

Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11:443–454

Jamnik P, Mahnič N, Mrak A, Pogačnik L, Jeršek B, Niccolai A, MastenRutar J, Ogrinc N, Dušak L, Ferjančič B, Korošec M, Cerar A, Lazar B, Lovše U, Pungert T, Fabjan P, PoklarUlrih N (2022) Fermented biomass of Arthrospira platensis as a potential food ingredient. Antioxidants 11:216

Jerković I, Cikoš AM, Babić S, Čižmek L, Bojanić K, Aladić K, Ul’yanovskii NV, Kosyakov DS, Lebedev AT, Čož-Rakovac R, Trebse P, Jokic S (2021) Bioprospecting of less-polar constituents from endemic brown macroalga Fucus virsoides J. Agardh from the Adriatic Sea and targeted antioxidant effects in vitro and in vivo (zebrafish model). Mar Drugs 19:235

Kumar SS, Devasagayam T, Bhushan B, Verma NC (2001) Scavenging of reactive oxygen species by chlorophyllin: an ESR study. Free Radic Res 35:563–574

Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278

Leandro A, Pereira L, Gonçalves AMM (2020) Diverse applications of marine macroalgae. Mar Drugs 18:17

Li Y-X, Wijesekara I, Li Y, Kim S-K (2011) Phlorotannins as bioactive agents from brown algae. Process Biochem 46(12):2219–2224. https://doi.org/10.1016/j.procbio.2011.09.015

Li HB, Cheng KW, Wong CC, Fan KW, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776

Li X, Qi Z, Zhao L, Yu Z (2016) Astaxanthin reduces type 2 diabetic associated cognitive decline in rats via activation of PI3K/Akt and attenuation of oxidative stress. Mol Med Rep 13:973–979

Markou G, Chentir I, Tzovenis I (2021) Microalgae and cyanobacteria as food: legislative and safety aspects. Cultured microalgae for the food industry. pp 249–264

Marsan DW, Conrad SM, Stutts WL, Parker CH, Deeds JR (2018) Evaluation of microcystin contamination in blue-green algal dietary supplements using a protein phosphatase inhibition-based test kit. Heliyon 4:e00573

Martínez-Ruiz M, Martínez-González CA, Kim D-H, Santiesteban-Romero B, Reyes-Pardo H, Villaseñor-Zepeda KR, Meléndez-Sánchez ER, Ramírez-Gamboa D, Díaz-Zamorano AL, Sosa-Hernández JE et al (2022) Microalgae bioactive compounds to topical applications products—a review. Molecules 27:3512. https://doi.org/10.3390/molecules27113512

Martins C, Vilarinho F, Sanches Silva A, Andrade M, Machado AV, Castilho MC, Sá A, Cunha A, Vaz MF, Ramos F (2018) Active polylactic acid film incorporated with green tea extract: development, characterization and effectiveness. Ind Crops Prod 123:100–110

Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y (1999) Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol 181:6571–6579

Mohamed ZA (2018) Potentially harmful microalgae and algal blooms in the Red Sea: current knowledge and research needs. Mar Environ Res. https://doi.org/10.1016/j.marenvres.2018.06.0

Mohamed ZA, Al-Shehri AM (2015) Biodiversity and toxin production of cyanobacteria in mangrove swamps in the Red Sea off the southern coast of Saudi Arabia. Bot Mar 58(1):23–34. https://doi.org/10.1515/bot-2014-0055

Mohamed Hatha AA, Sumayya NS (2023) Antioxidants from marine cyanobacteria. In: Kim S-K, Shin K-H, Venkatesan J (eds) Marine antioxidants. Academic Press, London, pp 119–131

Morone J, Alfeus A, Vasconcelos V, Martins R (2019) Revealing the potential of cyanobacteria in cosmetics and cosmeceuticals—a new bioactive approach. Algal Res 41:101541

Nagaoka S (2019) Yogurt production. Methods Mol Biol 1887:45–54

Ng HS, Chew LL (2023) Valuable compounds produced by microalgae. In: Bisaria V (eds) Handbook of biorefinery research and technology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6724-9_13-2

Niccolai A, Shannon E, Abu-Ghannam N, Biondi N, Rodolfi L, Tredici MR (2019) Lactic acid fermentation of Arthrospira platensis [Spirulina] biomass for probiotic-based products. J Appl Phycol 31:1077–1083

Nicoletti M (2022) The nutraceutical potential of cyanobacteria. Pharmacol. Potential Cyanobacteria. 2022:287–330. https://doi.org/10.1016/B978-0-12-821491-6.00010-7

Omatola CA, Okolo MLO, Adaji DM, Mofolorunsho CK, Oyiguh JA, Zige DV, Akpala NS, Samson SO (2020) Coinfection of human immunodeficiency virus-infected patients with hepatitis B virus in Lokoja, North Central Nigeria. Viral Immunol 33:391–395

Orona-Navar A, Aguilar-Hernández I, Nigam KDP, Cerdán-Pasarán A, Ornelas-Soto N (2021) Alternative sources of natural pigments for dye-sensitized solar cells: algae, cyanobacteria, bacteria, archaea and fungi. J Biotechnol 332:29–53

Osuna-Ruiz I, López-Saiz CM, Burgos-Hernández A, Velázquez C, Nieves-Soto M, Hurtado-Oliva MA (2016) Antioxidant, antimutagenic and antiproliferative activities in selected seaweed species from Sinaloa, Mexico. Pharm Biol 54:2196–2210

Pashkow FJ, Watumull DG, Campbell CL (2008) Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am J Cardiol 101:58–68

Patel A, Mishra S, Ghosh PK (2006) Antioxidant potential of C-phycocyanin isolated from cyanobacterial species Lyngbya, Phormidium and Spirulina spp. Indian J Biochem Biophys 43(1):25–31

Pekkoh J, Lomakool S, Chankham J, Duangjan K, Thurakit T, Phinyo K, Ruangrit K, Tragoolpua Y, Pumas C, Pathom-aree W, Srinuanpan S (2022) Maximizing biomass productivity of cyanobacterium Nostoc sp. through high-throughput bioprocess optimization and application in multiproduct biorefinery towards a holistic zero waste. Biomass Convert Biorefinery 1:1–21

Perković L, Djedović E, Vujović T, Baković M, Paradžik T, Čož-Rakovac R (2022) Biotechnological enhancement of probiotics through co-cultivation with algae: future or a trend? Mar Drugs 20:142

Pilipavicius V (ed) (2014) Organic agriculture towards sustainability. IntechOpen, London, pp 147–169. https://doi.org/10.5772/58239

Polyak YM, Sukharevich VI (2023) Problems and prospects of applications of cyanobacteria [Review]. Inland Water Biol 16:62–69

Radman S, Cikoš AM, Flanjak I, Babić S, Čižmek L, Šubarić D, Čož-Rakovac R, Jokić S, Jerković I (2021) Less polar compounds and targeted antioxidant potential [in vitro and in vivo] of Codium adhaerens C. Agardh 1822. Pharmaceuticals 14:944

Radman S, Čižmek L, Babić S, Cikoš AM, Čož-Rakovac R, Jokić S, Jerković I (2022) Bioprospecting of less-polar fractions of Ericariacrinita and Ericariaamentacea: developmental toxicity and antioxidant activity. Mar Drugs 20:57

Raja R, Hemaiswarya S, Arunkumar K, Carvalho IS (2016) Antioxidant activity and lipid profile of three seaweeds of Faro, Portugal. Revista Brasileira Botanica 39:9–17

Rajishamol MP, Lekshmi S, Vijayalakshmy KC, Saramma AV (2016) Antioxidant activity of cyanobacteria isolated from Cochin Estuary. Indian J Geo Mar Sci 45:974–977

Rizvi S, Raza ST, Ahmed F, Ahmad A, Abbas S, Mahdi F (2014) The role of vitamin E in human health and some diseases. Sultan Qaboos Univ Med J 14:e157

Romay C, Armesto J, Remirez D, Gonzalez R, Ledon N (1998) Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflamm Res J 47:36–41

Sakurai I, Mizusawa N, Wada H, Sato N (2012) Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol 160:1008–1017

Sies H (2017) Oxidative stress: concept and some practical aspects. Antioxidants 23:1191–1192

Singh DP, Prabha R, Meena KK, Sharma LS, Sharma AK (2014) Induced accumulation of polyphenolics and flavonoids in cyanobacteria under salt stress protects organisms through enhanced antioxidant activity. Am J Plant Sci 5:726–735

Singh R, Parihar P, Singh M, Bajguz A, Kumar J, Singh S, Singh VP, Prasad SM (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol 8:515

Singh RK, Tiwari SP, Rai AK, Mohapatra TM (2011) Cyanobacteria: an emerging source for drug discovery. J Antibiot 64:401–412

Singh S, Kate BN, Banerjee UC (2016) Bioactive compounds from cyanobacteria and microalgae: an overview. Crit Rev Biotechnol 36:146–158

Smerilli A, Balzano S, Maselli M, Blasio M, Orefice I, Galasso C, Sansone C, Brunet C (2019) Antioxidant and photoprotection networking in the coastal diatom Skeletonema marinoi. Antioxidants 8(6):154. https://doi.org/10.3390/antiox8060154

Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96

Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21:179–211

Suh SS, Hwang J, Park M, Seo HH, Kim HS, Lee JH, Moh SH, Lee TK (2014) Anti-inflammation activities of mycosporine-like amino acids (MAAs) in response to UV radiation suggest potential anti-skin aging activity. Mar Drugs 12(10):5174–5187. https://doi.org/10.3390/md12105174

Takaichi S (2004) Carotenoids and carotenogenesis in anoxygenic photosynthetic bacteria. In: The photochemistry of carotenoids, pp 39–69. https://doi.org/10.1007/0-306-48209-6_3

Tamang JP, Shin DH, Jung SJ, Chae SW (2016) Functional properties of microorganisms in fermented foods. Front Microbiol 7:578

Tamang JP, Watanabe K, Holzapfel WH (2016) Review: diversity of microorganisms in global fermented foods and beverages. Front Microbiol 7:377

Taylor JRN, Schober TJ, Bean SR (2018) Sorghum and millets: chemistry, technology, and nutritional attributes. Wiley-Blackwell, Hoboken

Tian F (2019) Introduction. In: Chen W (ed) Lactic acid bacteria. Springer, Singapore, pp 1–12

Uchida M, Miyoshi T (2013) Algal fermentation—the seed for a new fermentation industry of foods and related products. Jpn Agric Res Q 47:53–63

Vincent WF (2009) Cyanobacteria. In: Likens GE (ed) Encyclopedia of inland waters. Academic Press, Oxford, pp 226–232

Wang M, Yin Z, Sun W, Zhong Q, Zhang Y, Zeng M (2023) Microalgae play a structuring role in food: effect of spirulina platensis on the rheological, gelling characteristics, and mechanical properties of soy protein isolate hydrogel. Food Hydrocolloids 136:108244

Wang Z, Xu Z, Sun L, Dong L, Wang Z, Du M (2020) Dynamics of microbial communities, texture and flavor in Suan zuo yu during fermentation. Food Chem. https://doi.org/10.1016/j.foodchem.2020.12736

Watanabe F, Katsura H, Takenaka S, Fujita T, Abe K, Tamura Y, Nakatsuka T, Nakano Y (1999) Dried green and purple lavers [Nori] contain substantial amounts of biologically active vitamin B12 but less of dietary iodine relative to other edible seaweeds. J Agric Food Chem 47:2341–2343

Wu H, Niu H, Shao A, Wu C, Dixon BJ, Zhang J, Yang S, Wang Y (2015) Astaxanthin as a potential neuroprotective agent for neurological diseases. Mar Drugs 13:5750–5766

Xia S, Gao B, Li A, Xiong J, Ao Z, Zhang C (2014) Preliminary characterization, antioxidant properties and production of chrysolaminarin from marine diatom Odontella aurita. Mar Drugs 12:4883–4897. https://doi.org/10.3390/md12094883

Yang Q, Yao H, Liu S, Mao J (2022) Interaction and application of molds and yeasts in Chinese fermented foods. Front Microbiol 12:664850. https://doi.org/10.3389/fmicb.2021.664850

Yasin D, Zafaryab M, Ansari S, Ahmad N, Khan NF, Zaki A, Rizvi MMA, Fatma T (2019) Evaluation of antioxidant and anti-proliferative efficacy of Nostoc muscorum NCCU 442. Biocatal Agric Biotechnol 17:284–293

Yu J, Ma D, Qu S, Liu Y, Xia H, Bian F, Zhang Y, Huang C, Wu R, Wu J, You S, Bi U (2020) Effects of different probiotic combinations on the components and bioactivity of spirulina. J Basic Microbiol 60:543–557

Yuan JP, Peng J, Yin K, Wang JH (2011) Potential health-promoting effects of astaxanthin: a high-value carotenoid mostly from microalgae. Mol Nutr Food Res 55:150–165

Zeeshan M, Suhail S, Biswas D, Farooqui A, Arif JM (2010) Screening of selected cyanobacterial strains for phycochemical compounds and biological activities in vitro. Biochem Cell Arch 10:163–168