Bio-pigmentation and Biotechnological Implementations E-Book
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- Herausgeber: John Wiley & Sons
- Kategorie: Wissenschaft und neue Technologien
- Sprache: Englisch
Recent technological advances have provided unique opportunities for the exploration of alternatives to the industrial use of chemically produced synthetic colors. The most promising developments in this area have been in bio-pigmentation derived from microorganisms. This groundbreaking book reviews the current state of the science of bio-pigmentation, providing important insights into the molecular mechanisms of microbial biosynthesis of industrial pigments. Featuring contributions by leading researchers from both industry and academe, it explores the latest advances in the use of bio-pigments as safe, sustainable alternatives to chemically synthesized pigments, and provides extensive coverage the most promising sources of bio-pigments within the food, feed, and pharmaceutical industries. * Proposes microbial uniqueness of coloration in variety of food, feed and pharmaceuticals * Covers the basic science behind bio-pigmentation as well as the latest advances in the field * Describes detection strategies for screening and identifying color producing microorganisms under varying environmental conditions * Provides an exhaustive review of the literature on color producing extremophiles and offers fascinating insights into color production as a stress response in extremophiles * Explores microbial molecular mechanisms of color production, with special coverage of color production as secondary metabolites under environmental stress Bio-pigmentation and Biotechnological Implementations is required reading for professionals and post-doctoral students of microbiology, applied microbiology, food microbiology, food science, and food biochemistry. It is a valuable working resource for scientists working in color-dependent food, feed, and pharmaceuticals.
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Table of Contents
Cover
Title Page
Copyright
Dedication
List of Contributors
Introduction
Chapter 1: Introduction of Natural Pigments from Microorganisms
1.1 Introduction
1.2 Microbial Pigments from Eukaryotic Sources
1.3 Natural Pigments from Prokaryotes
1.4 Conclusion
References
Chapter 2: Establishing Novel Cell Factories Producing Natural Pigments in Europe
2.1 Introduction
2.2 Colorants
2.3 Screening for
Monascus
Pigment-Producing Cell Factories for the European Market
2.4 Assessment of the Color Yield
2.5 Optimizing Cellular Performance: Growth and Pigment Production
2.6 Pigment Properties
2.7 Conclusion
References
Chapter 3: Color-Producing Extremophiles
3.1 Introduction
3.2 Color-Producing Extremophiles
3.3 Microbial Pigments
3.4 Biotechnological Applications of Microbial Pigments from Extremophiles
3.5 Conclusion
Acknowledgments
References
Chapter 4: Current Carotenoid Production Using Microorganisms
4.1 Introduction
4.2 β-carotene
4.3 Lycopene
4.4 Astaxanthin
4.5 Zeaxanthin
4.6 Canthaxanthin
4.7 Torulene and Thorularhodin
4.8 Prospects for Carotenoid Production by Genetically Modified Microorganisms
4.9 Conclusion
References
Chapter 5: C50 Carotenoids: Occurrence, Biosynthesis, Glycosylation, and Metabolic Engineering for their Overproduction
5.1 Introduction
5.2 Occurrence and Biological Function of C50 Carotenoids
5.3 Biosynthesis of C50 Carotenoids
5.4 Glycosylation of C50 Carotenoids
5.5 Overproduction of C50 Carotenoids by Metabolic Engineering
5.6 Conclusion
Acknowledgments
References
Chapter 6: Biopigments and Microbial Biosynthesis of β-carotenoids
6.1 Introduction
6.2 Characterization of Biological Pigments
6.3 Biosynthetic Routes of β-carotene
6.4 Molecular Regulation of β-carotene Biosynthesis
6.5 Commercialization of β-carotene
6.6 Conclusion
References
Chapter 7: Biotechnological Production of Melanins with Microorganisms
7.1 Introduction
7.2 Microbial Production of Melanins
7.3 Production of Melanins with Engineered Microorganisms
7.4 Conclusion
References
Chapter 8: Biochemistry and Molecular Mechanisms of Monascus Pigments
8.1 Introduction
8.2
Monascus
Pigments
8.3 The Properties of
Monascus
Pigments
8.4 Functional Properties of
Monascus
Pigments
8.5 Biosynthetic Pathway of
Monascus
Pigments
8.6 Biosynthetic Pathway of Related Genes
8.7 Factors Affecting
Monascus
Pigment Production
References
Chapter 9: Diversity and Applications of Versatile Pigments Produced by Monascus sp
9.1 Introduction
9.2 Pigment-Producing
Monascus
Strains
9.3 Various Types of
Monascus
Pigments
9.4 Extraction and Purification of
Monascus
Pigments
9.5 Detection and Purification
9.6 Applications
9.7 Conclusion
Acknowledgments
References
Chapter 10: Microbial Pigment Production Utilizing Agro-industrial Waste and Its Applications
10.1 Introduction
10.2 Agro-industrial Waste Generation: A Scenario
10.3 Microbial Pigments
10.4 Production of Microbial Pigments Utilizing Agro-industrial Waste from Different Industries
10.5 Case Study: Production of Violacein by
Chromobacterium violaceum
Grown in Agricultural Wastes
10.6 Conclusion
Acknowledgments
References
Chapter 11: Microbial Pigments: Potential Functions and Prospects
11.1 Introduction
11.2 Potential Sources of Microbial Pigments
11.3 Physical Factors Influencing Microbial Pigments
11.4 Chemical Factors Influencing Microbial Pigments
11.5 Fermentation Practices in Pigment Production
11.6 Characterization and Purification Analysis
11.7 Biocolors from Microbes and their Potential Functions
References
Chapter 12: The Microbial World of Biocolor Production
12.1 Introduction
12.2 Pigments Produced by Microorganisms
12.3 Classification of Pigments
12.4 Benefits and Applications of Microbial Pigments
12.5 Conclusion
References
Index
End User License Agreement
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Guide
Cover
Table of Contents
Introduction
Begin Reading
List of Illustrations
Chapter 1: Introduction of Natural Pigments from Microorganisms
Figure 1.1 Structures of four representative carotenoids: β-carotene, lutein, canthaxanthin, and astaxanthin.
Figure 1.2 Nine representative fungal pigments: riboflavin, monascin, ankaflavin, rubropunctatin, monascorubramine, atrovenetin, herqueinone, bikaverin, and catenarin.
Figure 1.3 Structures of melanin and biliverdin.
Figure 1.4 Structures of phycocyanbilin and phycoerythrobilin.
Figure 1.5 Biosynthetic pathway of scytonemin.
Figure 1.6 Structures of five bacterial pigments: zeaxanthin, xanthomonadin I, prodigiosin, violacein, and actinorhodin.
Figure 1.7 Indigo (from plants) and indigoidine (from bacteria). (a) Structure of indigo. (b) Biosynthetic pathway of indigoidine.
Figure 1.8 Biosynthetic pathway of flaviolin.
Chapter 2: Establishing Novel Cell Factories Producing Natural Pigments in Europe
Figure 2.1 Percentage market share of food colorants in 2014 (Wissgott and Bortlik 1996).
Figure 2.2 Chemical structures of the original six Monascus pigments.
Figure 2.3 Monascus pigment biosynthesis based on a proposal by Balakrishnan
et al.
(2013).
Figure 2.4 Chemical structures of monascus pigment derivatives associated with
T. atroroseus
.
Figure 2.5 Major steps in the establishment of a successful cell factory.
Figure 2.6 Steps in product identification when establishing a novel cell factory.
Figure 2.7 Yellow, orange, and red UV spectra from three
Monascus
pigments: monascine (yellow), monascorubrine (orange), and rubropunctamine (red).
Figure 2.8 Interactions to consider when implementing novel cell factories for pigment production.
Chapter 3: Color-Producing Extremophiles
Figure 3.1 Representative environments of extremophiles. (a) Acid waters in Tinto River, Spain. (b) Red snow in Antarctica. (c) Stromatolites from Amarga Lagoon in Torres del Paine, Chile. (d) Uzon Caldera (e) and Geyser Valley, Kamchatka. (f) Salty environment in Santa Pola salterns, Spain.
Figure 3.2 Pigment synthesis at increasing temperature. Bacterial cultures of
S. oneidensis
(upper panel) and
S. frigidimarina
(bottom panel) incubated at 0, 4, 15, 20, and 30 °C. An intense reddish color can be observed in cells cultured at higher temperatures.
Figure 3.3 Cytochrome c3 protein network. Theoretical prediction obtained with String v. 10.0 (http://string-db.org) of the functional protein association network of cytochrome c3 from the antarctic bacteria
S. frigidimarina
.
Figure 3.4 Examples of the applications of pigments obtained from color-producing extremophiles. New environmental microorganisms are being isolated and cultured as a source of pigments used in the food, pharmaceutical, and textile industries, in environmental decontamination, in the research of laboratory tools, and in the development of microbial fuel cells.
Chapter 4: Current Carotenoid Production Using Microorganisms
Figure 4.1 Metabolic engineering of microbial carotenoid production.
Chapter 5: C50 Carotenoids: Occurrence, Biosynthesis, Glycosylation, and Metabolic Engineering for their Overproduction
Figure 5.1 Structures of C50 carotenoids and schematic representation of their biosynthesis, starting from lycopene and leading to (a) decaprenoxanthin in
C. glutamicum
, (b) sarcinaxanthin in
M. luteus
, (c) C.p. 450 in
Dietzia
sp. CQ4, (d) bacterioruberin in
H. japonica
, and (e) C50-lycopene and C50-astaxanthin in recombinant
E. coli
. IPP, isopentenyl pyrophosphate; DMAPP, dimethylallyl pyrophosphate; GPP, geranyl pyrophosphate; FPP, farnesyl pyrophosphate; GGPP, geranylgeranyl pyrophosphate; CrtB, phytoene synthase; CrtI, phytoene desaturase; CrtEb/CrtE2, lycopene elongase; CrtY
e/f
, C50 carotenoid ϵ-cyclase; CrtY
g/h
, C50 carotenoid γ-cyclase; LbtBC, lycopene elongase; LbtAB, C50 carotenoid β-cyclase; LyeJ, bifunctional lycopene elongase and 1,2-hydratase; CrtD, carotenoid 3,4-desaturase; CruF, C50 carotenoid 2-″,3-″-hydratase; FDS
Y81A,V157A
, farnesyl diphosphate synthase; CrtM
F26A,W38A,F233S
, carotenoid synthase; CrtIN304P, carotenoid desaturase; CrtY, lycopene cyclase; CrtW, β-carotene ketolase; CrtZ, β-carotene hydroxylase. For further abbreviations see text.
Chapter 6: Biopigments and Microbial Biosynthesis of β-carotenoids
Figure 6.1 The MVA pathway for the biosynthesis of β-carotene in bacteria, fungi, and animals.
Figure 6.2 The proposed biosynthetic pathway leading to β-carotene. The bacterial
crt
genes required for conversions that are listed here apply to both photosynthetic and nonphotosynthtic bacteria. DMAPP, dimethylallyl pyrophosphate; IPP, isopentenyl pyrophosphate; GPP, geranyl pyrophosphate; FPP, farnesyl pyrophosphate; GGPP, geranylgeranyl pyrophosphate; PPPP, prephytoene pyrophosphate.
Figure 6.3 Biosynthesis of β-carotene via the MEP pathway in cynobacteria, microalgae, photosynthetic bacteria, and plants.
Chapter 7: Biotechnological Production of Melanins with Microorganisms
Figure 7.1 Metabolic pathways and expressed genes related to melanin synthesis in engineered
Escherichia coli
. Dashed arrows indicate two or more enzyme reactions. Underlined genes were overexpressed from plasmids. PTS, phosphotransferase system glucose transport protein; G6P, glucose-6-phosphate; E4P, D-erythrose 4-phosphate; PEP, phosphoenolpyruvate; DAHP, 3-deoxy-D-arabino-heptulosonate 7-phosphate; HPP, 4-hydroxyphenylpyruvate; L-Tyr L-tyrosine; L-Phe, L-phenylalanine; L-Trp, L-tryptophan; tktA, gene encoding transketolase; aroGfbr, gene encoding feedback inhibition-resistant DAHP synthase; tyrC, gene encoding cyclohexadienyl dehydrogenase; pheACM, gene encoding chorismate mutase domain from chorismate mutase-prephenate dehydratase.
Chapter 8: Biochemistry and Molecular Mechanisms of Monascus Pigments
Figure 8.1 Chemical structure of major
Monascus
pigments.
Figure 8.2 Chemical structures of four kinds of water-soluble
Monascus
pigments.
Figure 8.3 Predicted biosynthetic pathways of
Monascus
pigments.
Figure 8.4 Predicted biosynthetic pathway of yellow pigments.
Figure 8.5 Predicted biosynthetic pathway of orange pigments.
Figure 8.6 Predicted biosynthetic pathway of red pigments.
Figure 8.7
Monascus
pigments synthetic gene cluster and predicted biosynthetic pathway in
M. rubber
.
Source
: Chen
et al.
(2015). Reproduced with permission of John Wiley & Sons.
Figure 8.8
Monascus
pigments synthetic gene cluster and predicted biosynthetic pathway in
M. pilosus
.
Source
: Balakrishnan
et al.
(2013). Reproduced with permission of Springer.
Figure 8.9 Schematic representation of
Monascus
pigment production by solid-state fermentation.
Figure 8.10 Schematic representation of
Monascus
pigment production by submerged fermentation.
Chapter 9: Diversity and Applications of Versatile Pigments Produced by Monascus sp
Figure 9.1 Structures of major
Monascus
pigments.
Figure 9.2 Structures of minor
Monascus
pigments.
Figure 9.3 Structures of citrinin and monacolins.
Chapter 10: Microbial Pigment Production Utilizing Agro-industrial Waste and Its Applications
Figure 10.1 Growth profile of
C. violaceum
in nutrient broth.
Figure 10.2 Effect of time on pigment production on
C. violaceum
.
Figure 10.3 Growth profile of
C. violaceum
in nutrient broth at 25, 30, and 37 °C.
Figure 10.4 Absorption spectrum of the violet pigment obtained at different incubation temperatures.
Figure 10.5 Time course of cell growth and pH profile of
C. violaceum
cultivated in nutrient broth, tryptic soy broth, peptone glycerol broth, and luria-bertani medium.
Figure 10.6 Violacein production by
C. violaceum
in complex media.
Figure 10.7 Color intensity of pigments in (a) liquid substrate and (b) solid substrate.
Figure 10.8 Pigment production by
C. violaceum
grown in SCB, SPW, molasses, and brown sugar supplemented with 10% (v/v) L-tryptophan in distilled water. SCB, sugar cane bagasse; SPW, solid pineapple waste; BS, brown sugar; M, molasses.
Figure 10.9 Violacein production in SCB.
Chapter 11: Microbial Pigments: Potential Functions and Prospects
Figure 11.1 Structures of bacterial pigments.
Figure 11.2 Structures of fungal pigments.
Chapter 12: The Microbial World of Biocolor Production
Figure 12.1 Some food-grade pigments of microorganism origin and their structures (Venil
et al.
2013).
Figure 12.2 Representation of various color-producing microorganisms on a Petri plate.
List of Tables
Chapter 2: Establishing Novel Cell Factories Producing Natural Pigments in Europe
Table 2.1 Potential Pigment Producers for the European Market
Table 2.2 Reported Optimal Process Conditions for
T. atroroseus
and Related Species
Chapter 3: Color-Producing Extremophiles
Table 3.1 Examples of Pigments from the Major Groups of Extremophiles
Table 3.2 Biotechnological Applications of Pigments from Extremophiles
Chapter 4: Current Carotenoid Production Using Microorganisms
Table 4.1 Sources of β-Carotene and β-Carotene-Containing Preparations
Table 4.2 Isomers Described in “β-Carotene” from Various Sources
Table 4.3 Comparison of the Chemical Compositions of Synthetic Lycopene, Lycopene from Tomatoes, and Lycopene from
Blakeslea Trispora
Table 7.4 Microbial Production of Pigments (Already in Use as Natural Colorants or with High Potential in this Field)
Chapter 5: C50 Carotenoids: Occurrence, Biosynthesis, Glycosylation, and Metabolic Engineering for their Overproduction
Table 5.1 C50 Carotenoid Production Systems
Chapter 6: Biopigments and Microbial Biosynthesis of β-carotenoids
Table 6.1 Major Microorganisms Used for Natural Carotenoid Production
Table 6.2 Optimized Fermentation Media for Microbial Synthesis of Carotenoids
Table 6.3 Major Patents Relating to the β-Carotene Biosynthetic Process and Manufacture
Chapter 7: Biotechnological Production of Melanins with Microorganisms
Table 7.1 Common Types of Melanins and their Precursor Compounds
Table 7.2 Comparison of Microbial Strains for the Production of Melanins
Table 7.3 Comparison of Engineered Microbial Strains for the Production of Melanins
Chapter 9: Diversity and Applications of Versatile Pigments Produced by Monascus sp
Table 9.1 Microorganisms Producing Monascus Pigments
Chapter 10: Microbial Pigment Production Utilizing Agro-industrial Waste and Its Applications
Table 10.1 Microorganisms and Inexpensive Substrates Used for Pigment Production
Table 10.2 Health Effects of Synthetic Pigments (Blanc 1998; Durán
et al.
2002)
Table 10.3 Biologically Active Pigmented Compound from Bacteria and their Market Potential (Dufossé 2009)
Table 10.4 Price Comparison for the Production of 50 L of Prodigiosin from
Serratia Marcescens
UTM1 Using a Synthetic Versus an Agricultural-Based Growth Medium (Venil
et al.
2013)
Table 10.5 Natural Pigments Produced by Bacteria (Malik
et al.
2012)
Table 10.6 Recommended Amounts of Arpink Red in Various Foodstuffs, According to the Codex Alimentarius Commission (Kumar
et al.
2015)
Table 10.7 Pigments from
Monascus
sp. (Kumar
et al.
2015)
Table 10.8 Production of Microbial Pigments Utilizing Agro-Industrial Waste (Panesar
et al.
2015)
Chapter 11: Microbial Pigments: Potential Functions and Prospects
Table 11.1 Historical Development of Microbial Pigments.
Source
: Information from Duffosé
et al.
(2005)
Table 11.2 Functions of Different Microbial Pigments.
Source
: Based on Information Acquired from Duffosé (2006), Duran
et al.
(2002), Mapari
et al.
(2005), Ray and Eakin (1975), Teixeria
et al.
(2012), and Venil
et al.
(2013)
Chapter 12: The Microbial World of Biocolor Production
Table 12.1 Pigment-Producing Microorganisms
Bio-Pigmentation and Biotechnological Implementations
Edited by
Om V. Singh
Division of Biological and Health Sciences University of Pittsburgh, Bradford, PA, USA
This edition first published 2017
© 2017 John Wiley & Sons, Inc.
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Library of Congress Cataloging-in-Publication Data
Names: Singh, Om V., editor.
Title: Bio-pigmentation and biotechnological implementations / [edited by] Om V. Singh.
Description: Hoboken, NJ : Wiley-Blackwell, 2017. | Includes bibliographical references and index.
Identifiers: LCCN 2017007261 (print) | LCCN 2017008051 (ebook) | ISBN 9781119166146 | ISBN 9781119166177 (Adobe PDF) | ISBN 9781119166184 (ePub)
Subjects: | MESH: Industrial Microbiology | Pigments, Biological | Biotechnology-methods
Classification: LCC QR53 (print) | LCC QR53 (ebook) | NLM QW 75 | DDC 571.5/38-dc23
LC record available at https://lccn.loc.gov/2017007261
Cover Design: Wiley
Cover Image: Courtesy of Om V. Singh
The editor gratefully dedicates this book to Daisaku Ikeda, Uday V. Singh, and Indu Bala in appreciation for their encouragement.
List of Contributors
Wan Azlina Ahmad
, Department of Chemistry, Faculty of Science, Universiti Teknologi Malaysia, Johor, Malaysia
P. Akilandeswari
, Department of Microbiology, Karpagam University (Karpagam Academy of Higher Education), Tamil Nadu, India
Alberto Alcázar
, Department of Investigation, Hospital Ramon y Cajal, Madrid, Spain
Claira Arul Aruldass
, Department of Chemistry, Faculty of Science, Universiti Teknologi Malaysia, Johor, Malaysia
Di Chen
, Henan University of Technology, Zhengzhou, China
Cristina Cid
, Microbial Evolution Laboratory, Center for Astrobiology (CSIC-INTA), Torrejón de Ardoz, Spain
Laurent Dufossé
, Laboratoire de Chimie des Substances Naturelles et des Sciences des Aliments, ESIROI Agroalimentaire, University of La Réunion, Ile de La Réunion, France
Eva García-López
, Microbial Evolution Laboratory, Center for Astrobiology (CSIC-INTA), Torrejón de Ardoz, Spain
Guillermo Gosset
, Departamento de Ingeniería Celular y Biocatálisis, Instituto de Biotecnología, National Autonomous University of Mexico, Cuernavaca, Mexico
Roshan Gul
, Department of Biotechnology, Maharishi Markandeshwar University, Mullana-Ambala, Haryana, India
Sabine A.E. Heider
, GSK Vaccines S.r.I., Siena, Italy
Nadja A. Henke
, Chair of Genetics of Prokaryotes, Faculty of Biology & CeBiTec, Bielefeld University, Bielefeld, Germany
Thomas Isbrandt
, DTU Bioengineering, Technical University of Denmark, Lyngby, Denmark
Sunil H. Koli
, School of Life Sciences, North Maharashtra University, Maharashtra, India; and North Maharashtra Microbial Culture Collection Centre (NMCC), North Maharashtra University, Maharashtra, India
Raman Kumar
, Department of Biotechnology, Maharishi Markandeshwar University, Mullana-Ambala (Haryana), India
Thomas Ostenfeld Larsen
, DTU Bioengineering, Technical University of Denmark, Lyngby, Denmark
Jennifer Lau
, Division of Biological and Health Sciences, University of Pittsburgh, Bradford, PA, USA
Ana María Moreno
, Microbial Evolution Laboratory, Center for Astrobiology (CSIC-INTA), Torrejón de Ardoz, Spain
Rosemary C. Nwabuogu
, Division of Biological and Health Sciences, University of Pittsburgh, Bradford, PA, USA
Satish V. Patil
, School of Life Sciences, North Maharashtra University, Maharashtra, India; and North Maharashtra Microbial Culture Collection Centre (NMCC), North Maharashtra University, Maharashtra, India
Petra Peters-Wendisch
, Chair of Genetics of Prokaryotes, Faculty of Biology & CeBiTec, Bielefeld University, Bielefeld, Germany
B.V. Pradeep
, Department of Microbiology, Karpagam University (Karpagam Academy of Higher Education), Tamil Nadu, India
Jiancheng Qi
, University of Alberta, Edmonton, Canada
Chandrashekhar D. Patil
, School of Life Sciences, North Maharashtra University, Maharashtra, India
Anil K. Sharma
, Department of Biotechnology, Maharishi Markandeshwar University, Mullana-Ambala (Haryana), India
Om V. Singh
, Division of Biological and Health Sciences, University of Pittsburgh, Bradford, PA, USA
Rahul K. Suryawanshi
, School of Life Sciences, North Maharashtra University, Maharashtra, India; and North Maharashtra Microbial Culture Collection Centre (NMCC), North Maharashtra University, Maharashtra, India
Gerit Tolborg
, DTU Bioengineering, Technical University of Denmark, Lyngby, Denmark
Chidambaram Kulandaisamy Venil
, Department of Chemistry, Faculty of Science, Universiti Teknologi Malaysia, Johor, Malaysia
Changlu Wang
, Tianjin University of Science and Technology, Tianjin, China
Siyuan Wang
, Department of Biological Engineering, Utah State University, Logan, UT, USA
Volker F. Wendisch
, Chair of Genetics of Prokaryotes, Faculty of Biology & CeBiTec, Bielefeld University, Bielefeld, Germany
Mhairi Workman
, DTU Bioengineering, Technical University of Denmark, Lyngby, Denmark
Fuchao Xu
, Department of Biological Engineering, Utah State University, Logan, UT, USA
Nur Zulaikha Binti Yusof
, Department of Chemistry, Faculty of Science, Universiti Teknologi Malaysia, Johor, Malaysia
Jixun Zhan
, Department of Biological Engineering, Utah State University, Logan, UT, USA
Introduction
Biological pigments are naturally occurring chemical compounds that impart certain colors. They serve a variety of functional purposes, such as absorbing ultraviolet (UV) light in order to promote photosynthesis, desorbing certain UV wavelengths to protect organisms from photo damage, and attracting organisms in order to promote mating or pollination. Color-based evaluation is essential, as it indicates fertility, nutritional value, flavor, toxicity, and food spoilage. Human society has incorporated knowledge of our instinctive color perceptions into marketing in order to increase the appeal of food items, pharmaceuticals, and cosmetics.
Artificial food colors and synthetic and natural pigments are used as color additives to augment or correct imperfections in a food's natural color, indicate artificially flavored foods and medicines, or enhance a food's visual appeal. Color additives are used to provide color to foods whose natural color would potentially degrade during shipment and storage when exposed to UV light and extreme changes in temperature and humidity. In these cases, artificial color additives whose chemical structures are stable and do not degrade under various conditions may be preferable for marketing purposes. The US Food and Drug Administration (FDA), under the Food, Drugs and Cosmetics (FD&C) Act, Title 21 of the Code of Federal Regulations (21 CFR 170.3 and 21 CFR 170.30), has approved color additives in food as “GRAS” (Generally Recognized as Safe). The “safe” amount of an artificial color is known as the acceptable daily intake (ADI), measured in parts per million (ppm), that industries are legally permitted to use in products. However, if organisms, specifically humans and animals, cannot metabolize artificial chemical compounds, then how much of a dose is considered “safe” for consumption remains questionable.
The quandary lies directly in the advantage provided by chemically stable compounds. Naturally occurring pigments are biological derivatives of organic compounds that can be metabolically or chemically broken down because they serve to synchronize with organismal demands. Artificial chemical colors, on the other hand, are derivatives of coal tar and petroleum, which cannot be degraded completely. Therefore, artificial pigments are potentially perilous to life because such chemical behaviors are asynchronous with biological function. Studies have shown that various artificial food colors are being linked to biological and neurological effects, such as attention deficit hyperactivity disorder (ADHD) in children and cancer.
Synthesizing bio-pigments through unique microbial metabolic pathways could be the most appropriate way to develop safe natural pigments for industrial use. Understanding the genetic sequences for the biosynthetic metabolites provides further insight into how genes can be manipulated in microorganisms in order to obtain higher yields of specific biological pigments. The broader impact of producing bio-pigments from microorganisms will affect food science, pharmacology, and biomedical practices.
This book aims to bridge the technology gap and focuses on exploring microbial diversity and the various mechanisms regulating the biosynthesis of bio-pigments. Chapter 1 (Wang et al.) presents a variety of microbial pigments from eukaryotic and prokaryotic sources and discusses their properties and applications. Based on the demand of consumers for natural food colorants, Tolborg et al. in Chapter 2 discuss novel cell factories producing natural pigments in Europe. Due to their extraordinary properties, certain organisms, called “extremophiles” (mostly bacteria and archaea, and a few eukaryotes), can thrive under harsh environmental conditions. Garcia-Lopez et al. in Chapter 3 summarize our current understanding of pigments from microbial extremophiles and their potential applications in biotechnology.
Commercial processes for carotenoid production are already being employed. Microorganisms, particularly filamentous fungi, seem to be promising producers of biosynthesized pigments, due to their chemical and color versatility and stability. In Chapter 4, Dufossé presents the facts on current carotenoid production using various microorganisms. In continuation, Heider et al. in Chapter 5 note that the commercial value of carotenoids was reported as $1.5 billion in 2014 and discuss the use of biosynthesis, glycosylation, and metabolic engineering to meet the demand.
Carotenoids are classified by number of isoprene units. In Chapter 6, Nwabuogu et al. predominantly focus on the biosynthesis of β-carotene and its derivative pigments. They also present the native bacterial and fungal species responsible for the biosynthesis of these pigments, along with the molecular elements that regulate β-carotene biosynthesis and fermentation strategies around commercialization.
Among nontraditional pigments, melanin constitutes a diverse group of pigments present in most biological groups. Melanin production is dependent mainly on the activity of enzymes from the tyrosinase and laccase protein families. Gosset, in Chapter 7, presents the advances made in melanin production from microorganisms toward process development.
Monascus pigments, derived from the genus Monascus, are promising as additional or alternative natural food pigments. Wang et al. in Chapter 8 discuss the biochemistry and molecular mechanisms of Monascus pigments. In continuation, Koli et al. in Chapter 9 discuss the diversity and applications of versatile pigments produced by Monascus sp.
Agro-industrial wastes (e.g., livestock waste, manure, crop residue, food waste, molasses, etc.) are high-impact feedstocks with particular utility in the production of pigments. In Chapter 10, Venil et al. discuss the impact of agro-industrial waste and its application in microbial pigment production. In continuation, in Chapter 11, Akilandeswari and Pradeep explore the potential functions of and prospects for microbial pigments. Finally, Gul et al. in Chapter 12 summarize the use of microorganisms in biocolor production.
This book, Bio-pigmentation and Biotechnological Implementations, is a collection of outstanding articles elucidating several broad-ranging areas of progress and challenge in the utilization of microorganisms as sustainable resources in bio-pigmentation. It will contribute to research efforts in the scientific community and to commercially significant work for corporate businesses. The aim is to establish long-term safe and sustainable forms of biopigments through microbial biosynthesis, with minimum impact on the ecosystem.
We hope readers will find these chapters interesting and informative for their research pursuits. It has been my pleasure to put together this book with Wiley-Blackwell. I would like to thank all of the contributing authors for sharing their quality research and ideas with the scientific community through this work.
Chapter 1Introduction of Natural Pigments from Microorganisms
Siyuan Wang, Fuchao Xu and Jixun Zhan
Department of Biological Engineering, Utah State University, Logan, UT, USA
1.1 Introduction
Pigments are widely used in a variety of industries. In the food industry, one of the most important goals is to develop foods that have an attractive flavor and appearance. Artificial food coloring using synthetic dyes can make foods more appealing and desirable. However, the safety of these dyes has been questioned. Recent research has linked synthetic food dyes to a number of potential health problems, such as cancer in animals and attention-deficit disorder in children (Potera 2010). Synthetic colorants are criticized for having these problems, and consumers are showing more and more interest in products that do not include artificial coloring agents. Therefore, various natural sources of food-grade colorants are in high demand. The textile industry also uses millions of tons of dyes, pigments, and dye precursors every year, and almost all of them are manufactured synthetically (Chequer et al. 2013). Synthetic dyes have serious limitations in that their production involves the use of toxic chemicals and can generate hazardous wastes, which is unfriendly to the environment and to human health (Khan et al. 2013).
Biological pigments are substances from biological sources that have a particular color, corresponding to their structure. They are found in plants, animals, and microbial organisms. Natural pigments have been long studied, but they are receiving increasing attention from industry because of the potential health and environmental concerns around synthetic dyes. Biological pigments from microbial cells are termed “microbial pigments.” In addition to their function as colorants, some microbial pigments are also used to promote human health, providing key nutrients or compounds required by the body. Some also have particular biological activities, such as anti-inflammatory, antibiotic, anticancer, and immunosuppressive properties (Soliev et al. 2011). Microbial pigments with fluorescence are used in laboratories to label antibodies (Mahmoudian et al. 2010). Some pigments can also be used to indicate the progress of specific reactions or to track pH changes through changes in their color (Venil et al. 2014). A large number of pigments are produced by various species of bacteria, yeasts, fungi, and algae, with colors including brown, black, red, orange, yellow, green, blue, and purple, and structures such as carotenoids, anthraquinones, flavonoids, and tetrapirroles. Different biosynthetic enzymes are involved in the biosynthesis of microbial pigments. For example, carotenoids are typically synthesized by terpene synthases, flavonoids are assembled by polyketide synthases (PKSs), and indigoidine – a bacterial blue pigment – is synthesized by a nonribosomal peptide synthetase. Microbial pigments are used for different purposes depending on their color property and biological function. This chapter covers a variety of microbial pigments from eukaryotic and prokaryotic sources and discusses their properties and applications.
1.2 Microbial Pigments from Eukaryotic Sources
The cells of eukaryotes such as plants, animals, and fungi contain a nucleus and other organelles. Eukaryotic microorganisms produce a lot of different pigments. Some representative pigments from these organisms are described in this section, categorized according to their source: algae, fungi, and yeasts.
1.2.1 Pigments from Algae
Algae produce a variety of pigments. The most commonly used in the industry is the carotenoid β-carotene (Figure 1.1). Carotenoids belong to the family of tetraterpenoids and are found in the chloroplasts and chromoplasts of plants, algae, fungi, and some bacteria (Asker et al. 2007). They are yellow, orange, and red pigments that can be used for coloration. β-carotene is a red-orange nonpolar pigment that can be obtained from Dunaliella salina, a kind of marine green microalga. The production of β-carotene in D. salina is affected by high salinity, temperature, and light intensity. A high β-carotene content in D. salina can help it protect itself from intense light and osmotic pressure in the ocean (Oren 2005). β-carotene is well known for its antioxidant activity and for its use as food supplement (Stargrove et al. 2008). It is commercially produced across the world, due to its widespread use (Oren 2005). The first company to manufacture and sell natural β-carotene, Betatene Ltd., was established in 1985 (Nelis and Deleenheer 1991). Production of β-carotene from D. salina is often seen in large open ponds located in or near salt lakes in Australia, the United States, and China.
Figure 1.1 Structures of four representative carotenoids: β-carotene, lutein, canthaxanthin, and astaxanthin.
Besides β-carotene, many other carotenoids are produced by microalgae. For example, lutein (Figure 1.1) is obtained from different green algae, such as Chlorella, Chlorococcum, Chlamydomonas, and Spongiococcum. Lutein is a red-orange pigment that is generally insoluble in water. For some time, it was widely used in chicken feeds to improve the color of broiler chicken skin and egg yolks (Philip et al. 1976). In the human body, lutein is concentrated in the macula. Some research has revealed that lutein protects eyes against oxidation (Berendschot et al. 2000; Malinow et al. 1980). Canthaxanthin (Figure 1.1), a dark red food coloring agent, is another example of a cartenoid produced by algae. Dictyococcus cinnabarinus was reported to produce it canthaxanthin in 1970. The final concentration of cellular canthaxanthin in this organism is 1.0–1.2 mg/g (Tuttobelll and Ranciag 1970). Astaxanthin (Figure 1.1) is a red terpene that is biosynthesized by Haematococcus pluviais with up to 2% dry weight quantity (Nonomura 1990). This compound is a food coloring agent approved by the US Food and Drug Administration (FDA).
Algae produce many other microbial pigments, including water-soluble green chlorophyll, blue phycocyanins, and red phycoerythrins, from Rhodophta, Cyanophta, and Cryptophyta, respectively (Telford et al. 2001). Halobacterium spp. have been found to be responsible for the red color in the Great Salt Lake, Dead Sea, and Lake Magadi (Oren 2005).
1.2.2 Pigments from Fungi
Fungi comprise a diverse group of eukaryotic organisms, including yeasts, molds, and mushrooms. Some fungi are known to produce color compounds with particular biological properties. Many fungal pigments possess ecological functions varying from providing protection against environmental stress to preventing photo-oxidation. Some pigments, such as flavins, can even act as cofactors in enzyme catalysis (Mapari et al. 2010).
Riboflavin (vitamin B2) is a yellow food colorant that is approved for use in many countries. It is also used in the clinic to treat neonatal jaundice (Bailey et al. 1997) and it has been reported to prevent migraine (Sandor et al. 2000). Its structure is shown in Figure 1.2. Many molds can be used to produce riboflavin through fermentation (Jacobson and Wasileski 1994; Santos et al. 2005; Stahmann et al. 2000). Ashbya gossypi has been widely used in the production of riboflavin, as it provides a high yield and good genetic stability. Its final riboflavin level can reach 15 g/L (Broder and Koehler 1980).
Figure 1.2 Nine representative fungal pigments: riboflavin, monascin, ankaflavin, rubropunctatin, monascorubramine, atrovenetin, herqueinone, bikaverin, and catenarin.
A variety of color compounds have been discovered from fungi. The same genus may produce different pigments. This is exemplified by Monascus. Monascus can be classified into four different species: M. pilosus, M. purpureus, M. ruberand and M. froridanus. Different Monascus species produce many different industrially important pigments with three colors: red, orange, and yellowish. For example, M. purpureus 192F produces the yellow pigments monascin and ankaflavin, the orange pigment rubropunctatin, and the red pigment monascorubramine (Figure 1.2). Monascorubramine is the major product. The pH and nitrogen source in the fermentation broth affect the composition and yield of the pigments. Supplementation of Monascus pigments as a coloring agent into food can provide novel flavors (Chen and Johns 1993). These fungal metabolites have also shown interesting biological activities. For example, monascin and ankaflavin are natural 5′ adenosine monophosphate-activated protein kinase (AMPK) activators and have shown hypolipidemic and anti-inflammatory activities (Hsu et al. 2013, 2014). The two compounds have been found to improve memory and learning ability in amyloid β-protein intracerebroventricular-infused rat by suppressing Alzheimer's disease risk factors (Lee et al. 2015). Anticancer, antiatherosclerotic, antiallergic, antioxidant, and antidiabetic properties have also been reported (Hsu and Pan 2014; Hsu et al. 2011, 2012, 2014; Lee et al. 2012).
While the most common method of pigment production from microbes on an industrial scale is submerged fermentation, an immobilized culture system or solid-state fermentation system can be used for Monascus fermentation, with rice cassava, corn, and oat as the substrates. Under this system, the carbon source, nitrogen source, pH, and temperature can be easily controlled during production (Chen and Johns 1993; Tuli et al. 2015). Blue light has also shown various effects on pigment production in Monascus (Chen et al. 2016; Wang et al. 2015).
Bikaverin (Figure 1.2) is a red pigment that comes from fungi such as Fusarium and Gibberella (Chelkowski et al. 1992; Zhan et al. 2007). It represents a medicinally relevant compound, having been found to possess strong antimicrobial activity against certain protozoa and fungi, as well as promising anticancer activity (Deshmukh et al. 2014; Zhan et al. 2007). It is a polyketide compound that is assembled by a nonreducing type I PKS from ten units of malonyl-CoA. Its production has been extensively studied. During production from Gibberella fujikuro, its production medium was determined by a fractional factorial design and tested in a fluidized bioreactor, with the pigment found to be produced at 6.83 g/L (Escamilla-Silva et al. 2001).
Atrovenetin and herqueinone (Figure 1.2) are two structurally related pigments from filamentous fungi such as Penicillium herquei (Narasimhachari and Ramaswami 1966; Narasimhachari and Vining 1963) and Penicillium atrovenetum (Neill and Raistrick 1957). These compounds belong to the family of polyketides. Atrovenetin is purified as yellow-orange plates. It is a deoxyherqueinone-type phenalenone that has characteristic color reactions. It is orange in sodium hydroxide, yellow in concentrated sulfuric acid (with an intense yellow-green fluorescence), and red-brown in ethanolic ferric chloride. It has shown potent antioxidant activity and can stabilize vegetable oils such as soybean, rapeseed, and palm oils (Ishikawa and Sada 1991; Ishikawa et al. 1991). Herqueinone is a red pigment from P. herquei. Recently, the herqueinone biosynthetic gene cluster was identified from the genome of P. herquei. A nonreducing PKS in this gene cluster named PhnA synthesizes the heptaketide backbone and cyclizes it into the angular, hemiketal-containing naphtho-γ-pyroneprephenalenone (Gao et al. 2016), which is subjected to additional tailoring to form herqueinone.
The aforementioned pigments are just the tip of the iceberg of microbial pigments that can be produced from fungi. Fungal pigments exhibit rich chemical and structural diversity, with different colors. Emericella represents another good example of the diversity of fungal pigments: epurpurins A–C can be isolated from Emericella purpurea, falconensins A–H from Emericella falconensis, and falconensones A1 and B2 from Emericella fructiculosa (Mapari et al. 2005; Ogasawara and Kawai 1997). Anthraquinone (octaketide) pigments such as catenarin (Figure 1.2), parietin, macrosporin, chrysophanol, cynodontin, helminthosporin, tritisporin, and erythroglaucin are polyketide compounds produced by Eurotium spp., Fusarium oxysporum, Curvularia lunata, Dermocybe sanguinea, Penicillium sp., and Drechslera spp. (Gessler et al. 2013; Zhan et al. 2004). Catenarin is a red compound that has been isolated from a variety of fungi, including Pyrenophora tritici-repentis (Wakulinski et al. 2003), Ventilago leiocarpa (Lin et al. 2001), Talaromyces stipitatus (van Eijk 1973), and marine sponge-associated fungus Eurotium cristatum (Lin et al. 2001). It is phytotoxic and has been proposed to cause the red smudge symptom and contribute to tan spot, an important foliar disease of wheat caused by P. tritici-repentis (Bouras and Strelkov 2008). Catenarin has been found to inhibit the growth of fungi accompanying P. tritici-repentis during the saprophytic phase of development, with Epicoccum nigrum as the most sensitive species (Wakulinski et al. 2003). A recent study showed that catenarin can prevent type 1 diabetes in non-obese diabetic mice via inhibition of leukocyte migration involving the MEK6/p38 and MEK7/JNK pathways (Shen et al. 2012). This pigment has also shown in vitro inhibition of DNA-dependent RNA polymerase from Escherichia coli (Anke et al. 1980).
Besides the structural diversity, fungal pigments demonstrate a wide range of applications in industry and in the clinic, and their use is thus not limited to coloring agents. While anthraquinone from D. sanguinea and other pigments from Trichoderma spp. are widely involved in the wool and silk fiber industry, a red anthraquinone isolated from Penicillium oxalicum has been reported to have anticancer effects when used in food supplements (Sardaryan 2002). Some pigments mentioned in the algae section, such as β-carotene, astaxanthin, and canthaxanthin, can be produced by some fungi as well. Given the huge reservoir of fungi and their complex metabolic networks, it is expected that more and more pigments will be discovered from them in the future.
1.2.3 Pigments from Yeasts
Yeasts are a good source of microbial pigments. Different yeast strains, such as Rhodotorula glutinis, Cryptococus sp., Phaffia rhodozyma, and Yarrowia lipolytica, are able to produce different microbial pigments (Buzzini 2001). R. glutinis is a good example of why the biotech industry is so interested in yeasts, as it can make a number of different high-value pigments, such as β-carotene, torulene, and torularhodin (Latha and Jeevaratnam 2010). Researchers have engineered the production of total carotenoids from this strain by ultraviolet (UV)-B radiation mutation, because the low production rate of the wild type limited its industrial application (Moline et al. 2012). R. glutinis is also rich in vitamins and fat, and its extract has thus been used in feeds to enrich their nutrition and to protect against fungal contamination (Buzzini 2001).
Another specific yeast worth mentioning here is the basidiomycetous P. rhodozyma, also known as “colorful odyssey.” P. rhodozyma was first isolated in the 1960s. Researchers first became interested in this pink yeast because of its ability to biosynthesize the economically important pigment astaxanthin. An efficient method for the isolation of this pigment from P. rhodozyma has been established (Johnson et al. 1978). In fact, it has been found that the production of astaxanthinin in P. rhodozyma protects the strain against reactive oxygen species (ROS) (Johnson 2003).
In addition to the previously mentioned microbial pigments, yeasts can biosynthesize other kinds of pigment as well. Melanin has been reported to be produced by Saccharomyces neoformans var. nigricans (Vinarov et al. 2003). “Melanin” (Figure 1.3) and “melanin-like pigment” are broad terms for the black pigments observed in various organisms, including yeasts and bacteria. The biosynthesis of melanin results from the oxidation of tyrosine. This group of pigments can efficiently dissipate UV radiation. Therefore, melanin is used to protect against UV radiation and reduce the risk of skin cancer (Brenner and Hearing 2008). Another yeast species, Y. lipolytica, has been reported to produce a brown microbial pigment from tyrosine. Based on the production of this pigment in Y. lipolytica, Carreira et al. (2001) were able to reveal the mechanism of pigment production from tyrosine in a yeast species. Biliverdin (Figure 1.3) is a green tetrapyrrolic bile pigment found in human and non-human animals. This compound has shown promising antimutagenic and antioxidant properties. It is generated from heme by heme oxygenase. It can be further converted to bilirubin by biliverdin reductase. Microorganisms, including yeasts, are known to produce this pigment as well. For example, it has been reported that Candida lipolytica produces biliverdin with glucose or hexadecane as the carbon source (Finogenova and Glazunova 1969). The gene responsible for the biosynthesis of biliverdin has been discovered in yeast. Though biliverdin's production yield is low in yeast, bioengineers have successfully cloned, optimized, and expressed it in engineered E. coli (Chen et al. 2012), which represents a scalable and more efficient production method.
Figure 1.3 Structures of melanin and biliverdin.
1.3 Natural Pigments from Prokaryotes
Prokaryotes are structurally simpler and have fewer metabolic pathways than eukaryotes. However, they are also known to produce a variety of metabolites with different colors. Pigments from cyanobacteria and other bacteria are discussed in this section.
1.3.1 Natural Pigments from Cyanobacteria
Cyanobacteria are a diverse and ubiquitous group of prokaryotes that were formerly called blue-green algae. Unlike other algae, cyanobacteria are unicellular organisms and lack a nucleus and other membrane-bound organelles. Thus, they belong to prokaryotes, and have some features similar to those of common bacteria.
Many cyanobacteria produce light-absorbing pigments such as chlorophylls, carotenoids, and phycobiliproteins. Separation of cyanobacterial pigments by chromatography has been reported (Merzlyak et al. 1983). Most photosynthetic pigments bind to specific proteins in cyanobacteria to form complexes. Phycocyanin (blue), allophycocyanin (red), and phycoerythrin (red) are representative phycobiliproteins from cyanobacteria such as Oscillatoria redekei. Phycocyanobilin (Figure 1.4) is a blue phycobillin that is present in allophycocyanin and phycocyanin, while phycoerythrobilin (Figure 1.4) is a red phycobillin from phycoerythrin. These water-soluble pigment–protein complexes possess a variety of pharmacological properties. For example, phycocyanin is known to have antioxidant, anti-inflammatory, hepatoprotective, and neuroprotective activities (Rajagopal et al. 1997b). Phycocyanin can be used as a natural dye and food additive, and has applications in the nutraceutical and pharmaceutical industries. It has also been proposed that phycocyanin may act as a nitrogen reserve that can be reused during nitrogen starvation (Allen and Smith 1969).
Figure 1.4 Structures of phycocyanbilin and phycoerythrobilin.
Scytonemin (Figure 1.5) is an extracellular pigment produced by various sheathed cyanobacteria, such as Scytonema myochrous, Calothrix sp., and Lyngbya aestuarii (Dillon and Castenholz 2003). It has a yellow-brown color. Scytonemin becomes green and red in oxidized and reduced states, respectively. This pigment is an effective, photostable UV shield in prokaryotes (Rastogi et al. 2013, 2015). Though it was discovered in 1849, its structure was not characterized until 1993. This compound contains novel indolic and phenolic subunits (Proteau et al. 1993). Its biosynthesis in Lyngbya aestuarii has been studied. Three enzymes, ScyA, ScyB, and ScyC, are involved in the biosynthetic pathway that converts L-tryptophan and p-hydroxyphenylpyruvic acid into scytonemin (Figure 1.5) (Balskus et al. 2011). In addition to its UV-blocking activity, scytonemin has also shown anti-inflammatory, anticancer, antiproliferative, and antioxidant activities. Thus, it has found applications in sunscreen and as a therapeutic agent. In addition, scytonemin can be used as a biosignature in searching for life on Mars and other planets (Mishra et al. 2015).
Figure 1.5 Biosynthetic pathway of scytonemin.
1.3.2 Natural Pigments from Bacteria
The pigments produced by bacteria are usually light-absorbing compounds. They are responsible for the colors displayed by the organisms that produce them (Rajagopal et al. 1997b). As an alternative to the synthetic pigments used in various industries (food, drinks, cosmetics, textiles, pharmaceuticals), bacterial pigments provide a promising avenue for various applications, because of their significantly better biodegradability, safety profile, health benefits, and compatibility with the environment.
Bacteria produce a variety of carotenoids. The ketocarotenoid pigments astaxanthin and canthaxanthin, described in Section 1.2.1, are widely distributed in nature. Astaxanthin, a red ketocarotenoid, exhibits health-promoting activities such as antioxidant and anti-inflammatory effects. A unique astaxanthin-producing bacterium (strain TDMA-17T) belonging to the family Sphingomonadaceae has been isolated (Asker et al. 2012a). Photosynthetic bacteria have also been reported to produce carotenoids. Bradyrhizobium sp. strain ORS278 can produce a higher quantity of canthaxanthin, and the pigment represents 85% of its total carotenoid content (Hannibal et al. 2000). Humans and animals must obtain carotenoids through their diet as they lack the ability to synthesize carotenoids (Sacchi 2013). Carotenoids are added to animal feed to improve the color of chicken skin, egg yolks, and salmon (Rajput et al. 2012). β-carotene and zeaxanthin (Figure 1.6), which belong to the carotene family, are produced by many bacteria, including Flavobacterium sp. and Paracoccus xanthinifaciens (Berry et al. 2003). Zeaxanthin, with a yellow color, is a promising nutraceutical with many applications in the feed, food, and pharmaceutical industries due to its powerful antioxidant property. Dalal Asker isolated two effective zeaxanthin-producing bacteria, strains TDMA-5T and -16T, from the families of Sphingobacteriaceae and Sphingomonadaceae, respectively (Asker et al. 2012b). These carotene pigments are essential to maintaining the yellow color of the retinal macula, which gives them the ability to act as a sunblock on certain parts of the retina.
Figure 1.6 Structures of five bacterial pigments: zeaxanthin, xanthomonadin I, prodigiosin, violacein, and actinorhodin.
The phytopathogenic genus Xanthomonas produces a group of carotenoid-like pigments called xanthomonadins. These yellow, water-insoluble pigments are brominated aryl-polyenes associated exclusively with the outer membrane of the bacterial cell wall. Studies have shown that xanthomonadins are associated with the protection of the producing strains against photobiological damage (Jenkins and Starr 1982; Poplawsky et al. 2000; Rajagopal et al. 1997a). The structure of xanthomonadin I (Andrewes et al. 1976) is shown in Figure 1.6.
The bright-red pigment prodigiosin (Figure 1.6) is a tripyrrole. It was first characterized from Serratia marcescens and has been shown to be localized in extracellular and cell-associated vesicles and in intracellular granules (Kobayashi and Ichikawa 1991). A wide variety of bacteria can produce prodigiosin-related metabolites, and S. marcescens is a major producer of prodigiosin (Furstner 2003). Prodigiosin has been found to provide significant protection against UV stress in Vibrio sp. DSM 14379 (Boric et al. 2011). Immunosuppressive and anticancer activities have been reported for different prodigiosin analogs and synthetic indole derivatives (Montaner and Perez-Tomas 2003; Pandey et al. 2007). Prodigiosin has also been reported to be an active component in preventing and treating diabetes mellitus, and it has some applications in this regard (Hwanmook et al. 2003). Prodigiosin shows a red color, which means it can be used to dye many fibers, including wool, nylon, acrylics, and silk (Alihosseini et al. 2008). Ahmad et al. (2012) tested prodigiosin for its dyeing efficiency in a number of different fabrics (pure cotton, pure silk, pure rayon, jacquard rayon, acrylic, cotton, silk satin, and polyester). The results suggest that it could be used to dye acrylic. They also evaluated the potential of prodigiosin in coloring candles, paper, and soap and to be used as ink. Translucent candles showed a more intense coloration than fluted varieties. Prodigiosin-dyed paper became substantially reduced in color upon exposure to both sunlight and fluorescent light (Ahmad et al. 2012).
Violacein (Figure 1.6) is a natural pigment with striking purple hues. It is produced by diverse genera of bacterial strains, including Collimonas and Duganella. It has strong antibacterial effects due to its function as a toxin guarding against diverse potential bacterial predators, which makes it a promising drug candidate against Staphylococcus aureus and other Gram-positive pathogens. It has also shown activities against various cancer cells (Choi et al. 2015). Because it is easy to visualize, production of violacein by C. violaceum has become a useful indicator of quorum-sensing molecules and their inhibitors (Burt et al. 2014). The production of violacein by Duganella sp. B2 has been studied. The concentrations of potassium nitrate, L-tryptophan, and beef extract, the volume in the flask, and the pH showed significant effects on the production yield. The yield of violacein by Duganella sp. B2 reached 1.62 g/L under optimal conditions (Wang et al. 2009).
Melanin is a negatively charged, high-molecular-weight polymer with a black, brown, or gray color. It is synthesized from polymerized phenolic and/or indolic compounds and is usually used in sunblock to protect the skin against UV radiation. It can be found in many bacteria, including Cryptococcus neoformans and Burkholderia cepacia (Nosanchuk and Casadevall 2006). Microbes that can produce melanin show a metal-chelating ability (McLean et al. 1998). In addition, melanin shows significant antioxidant activity (Plonka and Grabacka 2006).
Actinorhodin (Figure 1.6) is a benzoisochromanequinone polyketide antibiotic produced from Streptomyces coelicolor (Magnolo et al. 1991). It belongs to a class of aromatic polyketides synthesized by type II PKSs (Manikprabhu and Lingappa 2013). It can be used as a pH indicator, turning red below pH 8.5 and blue above.
Indigo (Figure 1.7a) is a widely used natural dye originally from plants such as Indigofera. Since the natural source for indigo is limited, chemical synthesis has become the most economic method of producing this dye. However, chemical synthesis requires harsh conditions and the use of a strong base, which is environmentally unfriendly. Indigoidine (Figure 1.7b) is a water-insoluble blue pigment that was first isolated from phytopathogenic Erwinia as a powerful radical scavenger that enables phytopathogens to tolerate oxidative stress, organic peroxides, and superoxides during the plant defense response due to its structure of carbon–carbon double bonds conjugated with a carbonyl group. This bacterial pigment shows a bright blue color similar to that of indigo. Several different strains are reported to produce it. Indigoidine is assembled from two units of L-glutamine by a nonribosomal peptide synthetase (e.g. IndC from Erwinia chrysanthemi and Streptomyces aureofaciens CCM 3239, BpsA from Streptomyces lavendulae and Sc-indC from Streptomyces chromofuscus ATCC 49982) (Figure 1.7b). Recently, an indigoidine biosynthetic gene cluster was located in the genome of S. chromofuscus ATCC 49982. The gene cluster is silent and consists of five open reading frames, called orf1, Sc-indC, Sc-indA, Sc-indB, and orf2. Sc-IndC was functionally characterized as an indigoidine synthase through heterologous expression of the enzyme in bothStreptomyces coelicolor CH999 and E. coli BAP1. The titer of indigoidine in E. coli BAP1 was reported to be 2.78 g/L under optimized conditions. Its production was dramatically increased (by 41.4%/3.93 g/L) when Sc-IndB was co-expressed with it in E. coli BAP1 (Yu et al. 2013). In order to further improve production, a glutamine synthetase gene was amplified from E. coli and co-expressed with Sc-indC and Sc-indB in E. coli BAP1. At 2.5 mM (NH4)2HPO4, the titer can reach 7.08 ± 0.11 g/L (Xu et al. 2015). This provides a green, efficient production process for this promising blue dye.
Figure 1.7 Indigo (from plants) and indigoidine (from bacteria). (a) Structure of indigo. (b) Biosynthetic pathway of indigoidine.
Flaviolin is a dark yellow-brown compound from bacteria. It is synthesized through a type III polyketide biosynthetic pathway (Figure 1.8). Sequencing of the genome of Streptomyces toxytricini NRRL 15443 revealed a type III polyketide biosynthetic gene cluster, which includes stts (type III PKS), stmo (monooxygenase), and two cytochrome P450 genes, stp450-1 and stp450-2. StTS is a type III polyketide synthase that is homologous to RppA, a 1,3,6,8-tetrahydroxynaphthalene (THN) synthase from Streptomyces griseus (Funa et al. 1999). When it was overexpressed in E. coli BL21(DE3), flaviolin was produced. StTS utilizes five units of malonyl-CoA to synthesize THN, which can be oxidized by StMO or air to generate flaviolin. UV irradiation test showed that expression of StTS in E. coli BL21(DE3) provides strong protection of the cells against UV radiation.
Figure 1.8 Biosynthetic pathway of flaviolin.
1.4 Conclusion
Microorganisms produce a variety of pigments – many more than have been discussed in this chapter. The structures and functions of some of these microbial pigments are well established, but many others still remain to be solved. It is important to discover and identify more pigments and understand their physical, chemical, and biological properties, in order to use them in industry. In comparison to pigments from other sources, such as animals and plants, the production of microbial pigments can be easily scaled up. The recent development of recombinant technology, synthetic biology, and metabolic engineering will further facilitate cost-effective production of microbial pigments for industrial applications.
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