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Microbial Ecology of the Cocoa Chain

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Microbial Ecology of the Cocoa Chain Microbial ecology of the cocoa chain Quality aspects and insight into heat-resistant bacterial spores Lídia Josélia Rebelo Lima Thesis commitee Promotor Prof. dr. ir. M. H. Zwietering Professor of Food Microbiology Laboratory of Food Microbiology Wageningen University Co-promotor Dr. ir. M. J. R. Nout Associate professor of Food Microbiology Laboratory of Food Microbiology Wageningen University Other members Prof. dr. L. de Vuyst, Vrije Universiteit Brussel Prof. dr. M. Kleerebezem, Wageningen University Dr. M. H. J. Wells-Bennik, Nizo food research B.V. Prof. dr. S. Brul, Universiteit van Amsterdam This research was conducted under the auspices of the graduate school of Voeding, Levensmiddelentechnologie, Agrobiotechnologie en Gezonheid (VLAG). Microbial ecology of the cocoa chain Quality aspects and insight into heat-resistant bacterial spores Lídia Josélia Rebelo Lima Thesis Submitted in partial fulfillment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M. J. Kropff, in the presence of the Thesis Committee appointed by the Doctorate Board to be defended in public on Monday 10 December 2012 at 1.30 p.m. in the Aula. Lima, L. Microbial ecology of the cocoa chain. Quality aspects and insight into heat-resistant bacterial spores 312 pp. Thesis, Wageningen University, Wageningen, NL (2012) With references, with summaries in Dutch and English ISBN 978-94-6173-433-4 Aos meus queridos pais e aos meus manos Table of Contents Abstract Abbreviations Chapter 1 Introduction and thesis outline 1 Chapter 2 Theobroma cacao L., “The food of the gods”: Quality determinants 23 of commercial cocoa beans, with particular reference to the impact of the fermentation Chapter 3 Quality and safety of commercial cocoa beans 71 Chapter 4 Microbiota of cocoa powder with particular reference to aerobic 95 thermoresistant spore-formers Chapter 5 Microbiota dynamics and diversity at different stages of cocoa bean 119 industrial processing to cocoa powder Chapter 6 Compositional and ultrastructural factors that make Bacillus subtilis 147 subsp. subtilis spores highly heat-resistant Chapter 7 Germination of highly heat-resistant Bacillus subtilis spores and 173 relevance for cocoa-derived products Chapter 8 Genomic biomarkers of growth temperature preferences and spore 193 heat-resistance: a meta-analysis with Firmicutes Chapter 9 General discussion and future perspectives 233 List of references 253 Summary 291 Samenvatting 295 Acknowledgements 299 List of publications 305 About the author 309 Overview of completed training activities 311 Abstract Cocoa beans (Theobroma cacao L.) are the basis for chocolate and cocoa powder production. The first step in the production of these food products consists of a spontaneous fermentation of the beans in the tropical producing countries, in order to allow the formation of the essential precursor compounds of the cocoa flavour. Following this stage, cocoa beans are industrially transformed into a range of different products. In the first part of this thesis, the state of literature of cocoa bean fermentation was revisited with the aim of interlinking post-harvest processing practices and characteristics of the fermenting microbiota, with the quality of commercial cocoa beans obtained. This literature survey resulted in the identification of a number of research needs that can be used to design agricultural and operational measures, towards improving the quality of commercial cocoa beans. The second part of this thesis addressed the occurrence, levels and diversity of bacterial Thermoresistant Spores (ThrS) in commercial cocoa powder and in cocoa being transformed to cocoa powder in an industrial setting. Thermoresistant Spores were defined as spores which survive a heat-treatment of at least 100°C for 10 min, as opposed to the standard treatment at 80°C for 10 min for Total Spores (TS) determination. It was found that strains of Bacillus licheniformis and of the B. subtilis complex were the predominant species in the ThrS library and that strains of B. subtilis complex, including B. subtilis subsp. subtilis formed the most heat-resistant spores in situ and in vitro. Interestingly, a high heat-resistant spore phenotype was associated with diverse genotypes. In addition, a strategy was devised in order to identify biomarkers of spore heat-resistance. The comparison of physicochemical and ultrastructural properties among spores of different heat-resistance allowed the identification of manganese as a potential physiological biomarker for B. subtilis subsp. subtilis spores heat- resistance. On the other hand, a study of various genomic features conducted across strains of the phylum of Firmicutes, did not yield genomic biomarkers related to spore high heat- resistant phenotype, suggesting the primary role of spore physicochemical composition and ultrastructural characteristics as determinant factors of spore differential heat-resistance. In conclusion, this study presents suggestions to delve into the functionality of the microbiota involved in cocoa bean fermentation and to improve the quality of commercial cocoa beans. Furthermore, it contributes towards the understanding of the ecology of high heat-resistant aerobic bacterial spores in the cocoa chain and provides knowledge regarding their heat-resistance. The data gathered in this thesis are useful input for predictive modelling and to assist in the production of safe and high quality food. Abbreviations AA Acetic Acid AAB Acetic Acid Bacteria AF Aflatoxin AFLP Amplified Fragment Length Polymorphism ANOVA Analysis of Variance AOAC Association of Official Analytical Chemists B Basionym BCCCA The Biscuit Cake Chocolate and Confectionary Alliance CA Citric Acid CBS Centraalbureau voor Schimmelcultures CCP Critical Control Point CFU Colony Forming Unit CMAA Cocoa Merchants’ Association of America COG Cluster of Orthologous Groups DGGE Denaturing Gradient Gel Electrophoresis DNA Deoxyribonucleic Acid DPA Pyridine-2,6-dicarboxylic acid (Dipicolinic acid) E Ethanol EU European Union F Fructose FAO Food and Agriculture Organization FCC Federation of Cocoa Commerce FDA Food and Drug Administration FFA Free Fatty Acid G Glucose GC Gas Chromatography GC-content Guanine plus Cytosine content GTM Gene-Trait Matching HACCP Hazard Analysis and Critical Control Points ICA International Confectionary Association ICCO International Cocoa Organization ICE Intercontinental Exchange ICP-AES Inductively Coupled Plasma Atomic Emission Spectrometry ISO International Organization for Standardization IUPAC International Union of Pure and Applied Chemistry HPLC High Performance Liquid Chromatography KD Kyte and Doolittle LA Lactic Acid LAB Lactic Acid Bacteria LC Liquid Chromatography M Mannitol MDS Metadata set MLR Multiple Linear Regression MS Mass Spectrometry NGS Next Generation Sequencing NIRS Near Infrared Spectroscopy NMR Nuclear Magnetic Resonance NOG Non Supervised Orthologous Groups OG Orthologous Group OMCL Orthologs Markov Cluster ORF Open Reading Frame OTA Ochratoxin PAH Polycyclic Aromatic Hydrocarbons PCR Polymerase Chain Reaction RDP Ribosomal Database Project RNA Ribonucleic Acid S Sucrose SA Succinic Acid SASP Small Acid Soluble Protein SFC Solid Fat Content SOO Saturated fatty acid, Oleic acid, Oleic acid SOS Saturated fatty acid, Oleic acid, Saturated fatty acid TAG Triacylglycerol TAM Total Aerobic Microorganisms ThrS Thermoresistant Spores TS Total Spores UHT Ultra-High Temperature UNCTAD United Nations Conference on Trade and Development UV Ultra Violet WW Wimley and White Chapter 1 Introduction and thesis outline Chapter 1 The cocoa chain Introduction Cocoa beans, the fruit seeds from the tropical tree Theobroma cacao L. (family Sterculiaceae) are the principal raw material for chocolate production (Figure 1). However, before being traded in the countries of origin, the beans must undergo post-harvest processing comprising opening of the fruit (botanically a pod), natural fermentation and drying (Schwan and Wheals, 2004) (Figure 2). After the post-harvest processing, the beans are transported to industrial plants, for chocolate and cocoa powder production as well as cocoa butter extraction. Thus, the cocoa bean chain can be considered to be divided into two stages: the post-harvest and the industrial processing. Figure 1. The cocoa pod and the cocoa bean. (A) Cocoa plantation in São Tomé and Príncipe. (B) Cocoa pods with different degrees of ripening. (C) Detail of the inside of a cocoa seed, where the white mucilaginous pulp surrounding the seed is visible. (D) Fermented and dried cocoa beans. Source: L. Lima. (See back cover for colour version) Cocoa bean fermentation is the process whereby cocoa beans are converted into a commodity which is suitable to produce chocolate and cocoa powder. Without this process raw and dried cocoa beans do not develop the typical cocoa flavour upon roasting (Afoakwa et al., 2008). The process of fermentation typically involves piling of cocoa beans, mainly by forming heaps or in a cascade of boxes, and allowing microorganisms naturally occurring in the environment to develop on the mucilaginous pulp surrounding the bean during a number of days. The primary 2 Introduction and thesis outline goal of cocoa bean fermentation is to bring about changes in the parenchyma cells of the seeds, in order to form the precursor compounds of the flavour (namely free amino acids, reducing sugars and peptides) (Afoakwa et al., 2008). Other (desirable) roles fulfilled by the
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