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Production and Extraction by Solid-State Fermentation. a Review View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Universidade do Minho: RepositoriUM Biotechnology Advances 29 (2011) 365–373 Contents lists available at ScienceDirect Biotechnology Advances journal homepage: www.elsevier.com/locate/biotechadv Research review paper Bioactive phenolic compounds: Production and extraction by solid-state fermentation. A review Silvia Martins a, Solange I. Mussatto a,⁎, Guillermo Martínez-Avila b, Julio Montañez-Saenz c, Cristóbal N. Aguilar b, Jose A. Teixeira a a Institute for Biotechnology and Bioengineering (IBB), Centre of Biological Engineering, University of Minho, Campus Gualtar, 4710–057, Braga, Portugal b Food Research Department, School of Chemistry, Autonomous University of Coahuila, Blvd. Venustiano Carranza S/N Col. República Oriente, 25280, Saltillo, Coahuila, Mexico c Department of Chemical Engineering, School of Chemistry, Autonomous University of Coahuila, Blvd. Venustiano Carranza S/N Col. República Oriente, 25280, Saltillo, Coahuila, Mexico article info abstract Article history: Interest in the development of bioprocesses for the production or extraction of bioactive compounds from Received 27 July 2010 natural sources has increased in recent years due to the potential applications of these compounds in food, Received in revised form 20 January 2011 chemical, and pharmaceutical industries. In this context, solid-state fermentation (SSF) has received great Accepted 21 January 2011 attention because this bioprocess has potential to successfully convert inexpensive agro-industrial residues, Available online 1 February 2011 as well as plants, in a great variety of valuable compounds, including bioactive phenolic compounds. The aim Keywords: of this review, after presenting general aspects about bioactive compounds and SSF systems, is to focus on the Solid-state fermentation production and extraction of bioactive phenolic compounds from natural sources by SSF. The characteristics of Agro-industrial residues SSF systems and variables that affect the product formation by this process, as well as the variety of substrates Plants and microorganisms that can be used in SSF for the production of bioactive phenolic compounds are reviewed Bioactive compounds and discussed. Phenolic compounds © 2011 Elsevier Inc. All rights reserved. Contents 1. Introduction — bioactive compounds .................................................. 365 2. Solid-state fermentation (SSF) ..................................................... 367 3. Uses of SSF for bioactive phenolic compounds production ........................................ 369 3.1. Phenolic content increase in food products ............................................ 369 3.2. Production and extraction of bioactive phenolic compounds from agro-industrial residues ...................... 369 3.3. Production and extraction of bioactive phenolic compounds from plants . ............................ 370 4. Concluding remarks and future perspective ............................................... 371 Acknowledgments.............................................................. 371 References ................................................................. 371 1. Introduction — bioactive compounds others. Flavonoids constitute the largest group of plant phenolics, accounting for over half of the eight thousand naturally occurring Bioactive compounds are extra nutritional constituents that natu- phenolic compounds (Harborne et al., 1999). Variations in substitution rally occur in small quantities in plant and food products (Kris-Etherton patterns to ring C in the structure of these compounds result in the et al., 2002). Most common bioactive compounds include secondary major flavonoid classes, i.e., flavonols, flavones, flavanones, flavanols, metabolites such as antibiotics, mycotoxins, alkaloids, food grade isoflavones, and anthocyanidins. Fig. 1 shows examples of the most pigments, plant growth factors, and phenolic compounds (Hölker common naturally occurring flavonoids. Similarly to the flavonoids, et al., 2004; Kris-Etherton et al., 2002; Nigam, 2009). Phenolic phenolic acids constitute also an important class of phenolic compounds compounds comprise flavonoids, phenolic acids, and tannins, among with bioactive functions, usually found in plant and food products. Phenolic acids can be divided in two subgroups according to their structure: the hydroxybenzoic and the hydroxycinnamic acids (Fig. 2). ⁎ Corresponding author. Tel.: +351 253 604 424; fax: +351 253 604 429. E-mail addresses: [email protected], [email protected] The most commonly found hydroxybenzoic acids include gallic, p- (S.I. Mussatto). hydroxybenzoic, protocatechuic, vanillic and syringic acids, while 0734-9750/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.biotechadv.2011.01.008 366 S. Martins et al. / Biotechnology Advances 29 (2011) 365–373 OH ISOFLAVONES FLAVANOLS HO O OH OH OH O OH O HOO HO OH O HO O OH OH O HO O O OH OH O OH OH OH OH Daidzein Catechin Daidzin Catechin gallate OH OH OH OH OH OH CH3 O HO O HO O HO O O HO O OH H3C O HO O O OH OH O OH OH OH OH Glycitein Glycitin Epigallocatechin Epicatechin OH OH OH OH O OH OH HO HO O HO O O HO O OH OH HO O O O O OH O OH OH OH OH OH OH O O Genistein Genistin OH OH OH OH Epicatechin gallate Epigallocatechin gallate OH FLAVONES FLAVONOLS HO O OH OH O OH O OH O O OH OH OH O HOO HOO OH O O HOO OH O OH OH OH HO OH OH OH Chrysin OH Rutin Kaempferol Quercetin OH O OH O OH O OH OH HOO HOO HOO OH OH Apigenin OH Luteolin OH Myricetin OH FLAVANONES ANTHOCYANIDINS HO OH HOHO + O OH HO O HOHO OH HO O OH O HO O OH HO Naringenin OH Cyanidin CH3 O OH O O O OH OH + O CH HO O HO 3 OH O O OH Naringin OH OH OH O Taxifolin OH Malvidin Fig. 1. Examples of naturally occurring flavonoids. S. Martins et al. / Biotechnology Advances 29 (2011) 365–373 367 HYDROXYBENZOIC ACIDS HYDROXYCINNAMIC ACIDS O O O O HO OH OH OH OH HO HO HO HO O OH OH OH H3C Gallic acid Protocatechuic acid Ferulic acid Caffeic acid O O O O O OH OH H3C OH OH HO HO O HO O HO CH H3C 3 Vanillic acid p-Hydroxybenzoic acid p-Coumaric acid Sinapic acid OH CH3 O O O OH O O HO OH O OH HO OH HO O O O HO OH OH CH 3 OH Ellagic acid Syringic acid Cinnamic acid Quinic acid O O O OH HO O HO O OH OH OH OH OH HO OH Gentisic acid Salicylic acid OH Chlorogenic acid Fig. 2. Examples of naturally occurring phenolic acids. among the hydroxycinnamic acids, caffeic, ferulic, p-coumaric and tation, more specifically by the solid-state fermentation technique. sinapic acids can be pointed out (Bravo, 1998). The current status of this technology, the microorganisms, substrates In the last few years, great attention has been paid to the bioactive and cultivation conditions affecting the phenolic compounds forma- compounds due to their ability to promote benefits for human health, tion are summarized and discussed. such as the reduction in the incidence of some degenerative diseases like cancer and diabetes (Conforti et al., 2009; Kim et al., 2009), reduction 2. Solid-state fermentation (SSF) in risk factors of cardiovascular diseases (Jiménez et al., 2008; Kris-Etherton et al., 2002), antioxidant, anti-mutagenic, anti-allergenic, Fermentation processes may be divided into two systems: anti-inflammatory, and anti-microbial effects (Balasundram et al. 2006; submerged fermentation (SmF), which is based on the microorgan- Ham et al. 2009; Parvathy et al. 2009), among others. Due to these isms cultivation in a liquid medium containing nutrients, and solid- countless beneficial characteristics for human health, researches have state fermentation (SSF), which consists of the microbial growth and been intensified aiming to find fruits, vegetables, plants, agricultural and product formation on solid particles in the absence (or near absence) agro-industrial residues as sources of bioactive phenolic compounds. of water; however, substrate contains the sufficient moisture to allow Usually, bioactive compounds are recovered from natural sources by the microorganism growth and metabolism (Pandey, 2003). In recent solid–liquid extraction employing organic solvents in heat-reflux years, SSF has received more interest from researchers since several systems (Martins et al., 2010; Wang and Weller, 2006). However, studies have demonstrated that this process may lead to higher yields other techniques have been recently proposed to obtain these and productivities or better product characteristics than SmF. In compounds including the use of supercritical fluids, high pressure addition, due to the utilization of low cost agricultural and agro- processes, microwave-assisted extraction and ultrasound-assisted industrial residues as substrates, capital and operating costs are lower extraction (Cortazar et al. 2005; Markom et al. 2007; Wang and Weller, compared to SmF. The low water volume in SSF has also a large impact 2006). Extraction/production of bioactive compounds by fermentation on the economy of the process mainly due to smaller fermenter-size, is also an interesting alternative that merits attention, since it is able to reduced downstream processing, reduced stirring and lower sterili- provide high quality and high activity extracts while precluding any zation costs (Hölker and Lenz, 2005; Nigam, 2009; Pandey, 2003; toxicity associated to the organic solvents. In this process, bioactive Raghavarao et al., 2003). The main drawback of this type of cultivation compounds are obtained as secondary metabolites produced by concerns the scaling-up of the process,
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