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Cranfield University Nik Iskandar Putra Bin CRANFIELD UNIVERSITY NIK ISKANDAR PUTRA BIN SAMSUDIN POTENTIAL BIOCONTROL OF FUMONISIN B1 PRODUCTION BY FUSARIUM VERTICILLIOIDES UNDER DIFFERENT ECOPHYSIOLOGICAL CONDITIONS IN MAIZE APPLIED MYCOLOGY GROUP CRANFIELD SOIL AND AGRIFOOD INSTITUTE SCHOOL OF ENERGY, ENVIRONMENT AND AGRIFOOD PHD THESIS Academic Year: 2012-2015 Supervisor: PROF NARESH MAGAN, DSC October 2015 CRANFIELD UNIVERSITY APPLIED MYCOLOGY GROUP CRANFIELD SOIL AND AGRIFOOD INSTITUTE SCHOOL OF ENERGY, ENVIRONMENT AND AGRIFOOD PHD THESIS Academic Year: 2012-2015 NIK ISKANDAR PUTRA BIN SAMSUDIN POTENTIAL BIOCONTROL OF FUMONISIN B1 PRODUCTION BY FUSARIUM VERTICILLIOIDES UNDER DIFFERENT ECOPHYSIOLOGICAL CONDITIONS IN MAIZE Supervisor: PROF NARESH MAGAN, DSC October 2015 This thesis is submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy © Cranfield University 2015 All rights reserved. No part of this publication may be reproduced without the written permission of the copyright owner ABSTRACT Fusarium verticillioides contaminates maize with the fumonisin group of mycotoxins for which there are strict legislative limits in many countries including the EU. The objectives of this project were (a) to examine the microbial diversity of maize samples from different regions and isolate potential biocontrol agents which could antagonize F. verticillioides and reduce fumonisin B1 (FB1) production, (b) to screen the potential biocontrol candidates using antagonistic interaction assays and different ratios of inoculum on maize-based media and on maize kernels to try and control FB1 production, (c) to examine whether the potential control achieved was due to nutritional partitioning and relative utilization patterns of antagonists and pathogen, and (d) to examine the effects of best biocontrol agents on FUM1 gene expression and FB1 production on maize cobs of three different ripening stages. The total fungal and bacterial loads on maize from Malaysia, Mexico and France showed that the largest populations were on the former samples because of its high water content, regardless of the selective media used. The main fungal genera were Fusarium, Aspergillus and Penicillium based on frequency of isolation on different selective media. Other zygomycetes (Rhizopus, Mucor) and common soil fungi (Phoma, Kabatiella) were also isolated. A mycotoxigenic strain of F. verticillioides (FV1) was isolated from Malaysian maize kernels, and its identity confirmed molecularly. FV1 was used in all subsequent experiments. The effect of aw temperature on FV1 growth and FB1 production was determined and found to be similar to reference strains. A total of six microbial strains were screened. Interaction assays, growth and FB1 inhibition showed that BCAs 1, 4, 5 and 6 were effective. Studies of different pathogen:antagonist inoculum ratios showed that both on maize-based media and on maize kernels BCA1 (Clonostachys rosea 016) completely inhibited FB1 production at 25:75 inoculum ratio at 0.98 aw. BCA5 (a Gram-negative motile bacterium) was also effective, and utilized in subsequent studies. In all treatments, FB1 production was higher at 0.95 aw when compared to 0.98. i The mechanism of action was examined by comparing C-source utilization patterns in the Niche Overlap Index (NOI) and Temporal Carbon Utilization Sequence (TCUS) studies. It was found that aw temperature had significant impacts on C-source utilization patterns by BCA1 and BCA5 when compared with FV1. BCA1 and FV1 occupied similar niches at 0.95 aw+30°C and 0.98 aw+25°C. Despite repeated attempts, BCA5 was unable to grow in PEG 600 modified C-source media, possibly due to its toxicity effects. Subsequently, studies were carried out on maize cobs of different maturities. To this end, a q-PCR method was used to examine effect of the BCAs on relative FUM1 gene expression, and FB1 production was quantified by HPLC-FLD. Temporal studies on maize kernels showed that optimum FUM1 expression and FB1 production occurred after 10 days at both 0.95 and 0.98 aw. Aw temperature had significant impacts on growth, FUM1 gene expression and FB1 production by FV1 on maize cobs of different maturities. When using 50:50 pathogen:antagonist inoculum ratio, BCA1 significantly reduced FB1 levels on maize cobs by >70% at 25°C, and almost 60% at 30°C regardless of maize ripening stage. For BCA5, FB1 levels on maize cobs were significantly decreased in some treatments only. ii ACKNOWLEDGEMENTS “…bismillahir-rahmanir-rahim…” This thesis represents three long but well-spent years of hard work and steep learning curve in the field of Food Mycology. In making that hard work possible, and subsequently the writing and publication of this thesis, I am thus hugely indebted to my employer; Universiti Putra Malaysia (UPM), and to my sponsor; the Malaysian Ministry of Higher Education (MOHE), for giving me this opportunity. I also wish to convey my deepest appreciation to Prof. Naresh Magan, DSc, (main supervisor) and Dr. Angel Medina-Vaya (co-supervisor) as well as the members of my research supervisory committee; Dr. Nicola White (Chair), and Prof. Leon A. Terry (Assessor) for their intellectual counsel, experimental wisdom, editorial critiques, and technical recommendation which have immensely facilitated the framing and materializing of my PhD research. My heartfelt admiration goes to my family and friends who have stood by me through all these years with unceasing encouragement and genuine inspiration without which I would never have had what it needed to reach the finishing line. To Dr. Ronnie J. W. Lambert, FRSC, for his lessons on statistical analyses; Dr. Yousef Sultan of National Research Centre, Egypt, for his instruction on HPLC; and Dr. Alicia Rodriguez Jimenez of University of Extremadura, Spain, for her assistance on molecular biology; I express my profound gratitude. Finally, to all members of Applied Mycology Group, Cranfield Soil and AgriFood Institute, I thank you all for the time, help, laughter and late night sessions in the laboratory that we have shared on so many occasions. All of you and those memories will in fact be an integral part of my future success, and will be greatly missed. My experience at Cranfield University has been very pleasant and heart-warming. “...in God we trust, with Knowledge we progress, by Love we live...” iii “…the Time spent, the Knowledge acquired, the Wisdom attained and the subsequent Thoughts herein documented are affectionately dedicated to my loving parents and siblings…” iv TABLE OF CONTENT Abstract i Acknowledgements iii Dedication iv Table of Content v List of Tables xii List of Figures xvi List of Equations xx List of Abbreviations xxi List of Symbols xxii List of Appendices xxiii CHAPTER 1 General introduction, literature review and research objectives 1.1 GENERAL INTRODUCTION 1 1.2 LITERATURE REVIEW 1.2.1 Maize; nutritional importance, human consumption and life cycle 5 1.2.2 Infection and diseases in maize 11 1.2.3 Fusarium verticillioides in maize; life cycle and dynamics of infection 14 1.2.4 Fumonisins; production by Fusarium verticillioides, toxicity in humans and animals, and regulatory limits 21 1.2.5 Ecophysiology of Fusarium verticillioides during growth, maize colonization and fumonisins production 28 1.2.6 Expression of FUM gene cluster and production of fumonisins as a secondary metabolite in Fusarium verticillioides 34 1.2.7 Potentials for biocontrol of Fusarium verticillioides in maize 38 v 1.3 RESEARCH AIMS AND OBJECTIVES 44 CHAPTER 2 Biodiversity of mycobiota in maize samples from different regions 2.1 INTRODUCTION 49 2.2 MATERIALS AND METHODS 2.2.1 Sampling of maize kernels 51 2.2.2 Measurement of water content and water activity of maize samples 51 2.2.3 Preparation of growth media for microbial cultivation 52 2.2.4 Fungal isolation, enumeration, and identification 54 2.2.5 Isolation and molecular identification of the Malaysian strain of Fusarium verticillioides FV1 56 (a) DNA Extraction 57 (i) Mechanical disruption of fungal mycelium 58 (ii) Cellular lysis by CTAB buffer 58 (iii) Phase separation by chloroform 59 (iv) DNA precipitation 59 (b) PCR amplification 60 (c) Gel electrophoresis 62 2.2.6 Fumonisin production of the Malaysian strain of Fusarium verticillioides FV1 and other reference strains on a Fumonisin- inducing Medium (FIM) 64 2.2.7 Ecophysiological studies of the Malaysian strain of Fusarium verticillioides FV1 on milled-maize agar (MMA) 66 2.2.8 Statistical analysis 68 2.3 RESULTS 2.3.1 Water content and water activity of maize kernel samples 70 vi 2.3.2 Isolation frequency and fungal populations in maize kernel sample 70 2.3.3 Isolation and molecular identification of Fusarium verticillioides FV1 73 2.3.4 Comparison of fumonisin production by Fusarium verticillioides FV1 and two reference strains on a fumonisin-inducing medium (FIM) 76 2.3.5 Effect of water activity temperature on growth and fumonisin B1 production by Fusarium verticillioides FV1 on milled-maize agar (MMA) 77 2.4 DISCUSSION 2.4.1 Biodiversity of mycobiota in maize kernel samples from different regions 79 2.4.2 Effect of interacting ecophysiological factors on growth and Fumonisin B1 production by Fusarium verticillioides FV1 on milled-maize agar (MMA) 81 2.5 CONCLUSIONS 82 CHAPTER 3 Efficacy of potential biocontrol agents for control of Fusarium verticillioides FV1 and fumonisin B1 under different inoculum ratios and water activities on milled- maize agar and stored maize kernels 3.1 INTRODUCTION 84 3.2 MATERIALS AND METHODS 3.2.1 Microorganisms 86 3.2.2 Isolation
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