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Molecular Characterisation of Antibiotic-Resistant Bacteria from Selected Water Distribution Systems in Southwestern Nigeria

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Molecular Characterisation of Antibiotic-Resistant Bacteria from Selected Water Distribution Systems in Southwestern Nigeria MOLECULAR CHARACTERISATION OF ANTIBIOTIC-RESISTANT BACTERIA FROM SELECTED WATER DISTRIBUTION SYSTEMS IN SOUTHWESTERN NIGERIA By Ayodele Timilehin ADESOJI B. Sc. Microbiology (Ife), M. Sc. Environmental Microbiology (Ibadan) Mat no: 142711 A Thesis in the Department of Microbiology Submitted to the Faculty of Science in Partial Fulfillment of the requirement for the Degree of Doctor of Philosophy of the University of Ibadan May, 2014 i Abstract The presence of Antibiotic-Resistant Bacteria (ARB) in water sources and treated drinking water is an emerging public health issue. Antibiotic resistance genes and mobile genetic elements (integron and gene cassettes) have been reported as bases of resistance in ARB. Available data on ARB in southwestern Nigeria are based on phenotypic studies. Information on molecular basis of resistance in ARB is necessary to determine the mode of resistance transfer among bacteria. This research was therefore aimed at molecular characterisation of ARB in water distribution systems of dams in Southwestern Nigeria. Ninety-six water samples were purposively collected aseptically into sterile screw cap bottles from six selected water distribution systems of dams in Ife, Ede, Asejire, Eleyele, Owena- Ondo and Owena-Idanre in Southwestern Nigeria. Samples were collected four times between December 2010 and July 2011 from raw, treated and two randomly selected municipal distribution taps. Bacteria were isolated from water samples and characterised using 16S rDNA sequencing. Antibiotic susceptibility of isolates was determined using point inoculation method. Multi-Drug Resistant (MDR) bacteria were selected based on resistance to over three classes of antibiotics and resistance genes were characterised by PCR and microarray analysis. Class 1 integron was detected by PCR while variable regions of integrase positive isolates were sequenced to identify inserted gene cassettes. Data were analysed using descriptive statistics and ANOVA at p=0.05. A total of 292 bacteria isolates were obtained. The highest (11.0%) bacteria occurrence was from Owena-Idanre raw water while the lowest (0.3%) was obtained from Eleyele treated water. They were identified as α-proteobacteria (4), β-proteobacteria (39), γ-proteobacteria (131), bacteroidetes (4), actinobacteria (2), firmicutes (105) and uncultured bacteria (7). Resistance to tetracycline, sulfamethoxazole, ampicillin and streptomycin among the 191 found to be MDR bacteria were 62.8, 93.7, 90.0 and 52.8 % respectively. Significant variation was observed between percentage of MDR bacteria in Owena-Idanre dam (12.6%) and those from Ife dam (4.2%). The most frequent resistance genes detected among MDR b bacteria were ant(3’) (56/101), blaTEM (59/172), sul 2 (51/179) and tetA (23/120). The highest incidence of ant(3’)b (12.5%) was found among bacteria obtained from Eleyele raw water while tetA (13.0%) was from Owena-Ondo treated water. Other antibiotic resistance genes such as floR, tetJ, tetH, StrB, qnrA1, dfrA21 and aadE from bacteria isolated in Asejire treated water and Owena-Idanre municipal taps were detected with Microarray. Class 1 integron was found in 42 bacteria with the highest frequency (14.3%) in Eleyele raw water ii while 2.4% each were obtained from Ede, Asejire and Eleyele municipal taps. Variable region was detected from 69.0% of bacteria carrying class 1 integron. Gene cassettes identified in the variable region of class 1 integron include aadA1, bla CTX-M, dfrA, Sul 1 and qnr A1 encoding resistance to aminoglycoside, extended β-lactams, trimethoprim, sulfamethoxazole and quinolones respectively. The presence of multi-drug resistant bacteria carrying different antibiotic resistance genes, integrons and gene cassettes as revealed by molecular characterisation, in the water distribution systems could facilitate the transfer of antibiotic resistance among bacteria of public health significance, hence the need for surveillance. Keywords: Water distribution systems, Multi-drug resistant bacteria, Integrons and gene cass ettes, Antibiotic resistance genes, Microarray gene detection Word count: 497 iii Acknowledgements My gratitude goes to the Almighty God the author and finisher of my faith. He gave me this vision and when I could not foresee its accomplishment. With His help and support He opened doors and of breakthroughs that saw to the completion of the study. I am very grateful to my supervisor Dr. A. A. Ogunjobi for his moral support and for painstakingly critiquing the work. I sincerely appreciate the Head of Department of Microbiology of this University Prof. O. E. Fagade who always encouraged me to work hard work. I appreciate Prof. A. A. Onilude and Dr. A. M. Salam for your fatherly advice and I also appreciate all lecturers and postgraduate students in the Department of Microbiology, University of Ibadan. I am very grateful to Dr. Femi Olatoye who supported me a great deal toward the success of this work. My gratitude also goes to Dr. Call Douglas, a distinguished Professor at Paul G. Allen School of Global Animal Health at Washington State University United States of America. He was magnanimous enough to accommodate and sponsor me in his laboratory for six months. Words cannot express how much I appreciate his assistance. I appreciate Dr. Guy Palmer for providing me with the invitation letter to Call’s Laboratory; Lisa Lorfe my diligent laboratory manager for her forbearance and assistance in spite of my inquisitions; as well as my entire laboratory mates for their hospitality. I also appreciate the various assistance friends like Theresa, Vaughn, Cornelius, Pastor Deji Arogundade and many others offered me during my stay at Washington State University. I am grateful to Dr. O. E. Adeleke the Head of the Department of Pharmaceutical Microbiology, University of Ibadan, for permitting me to conduct my bacteria isolation in his Department’s laboratory. Sincere gratitude also goes to the lecturers, postgraduate students and technical staff members of his Department. I appreciate the Dean of the Faculty of Science and Education, Prof. J.O. Fatokun, the Head of the Department of Biological Sciences, Dr. Alexandra Bem, and the entire members of staff of Federal University Dutsin-Ma, Katsina State where I lecture, for their unrelenting moral support. I also appreciate the University administration for granting me one year study fellowship leave for the completion of my PhD. These acknowledgements will not be complete without appreciating my parents Prof. and Mrs. F. A. Adesoji, for their uninterrupted moral and financial support. It is my prayer that the Lord God will continually grant you long life and good health to enjoy the fruits of your labour. I appreciate my siblings for their patience and understanding during the course of this iv study. Pelumi, Dotun, Taye and Kehinde, I love you all. I also appreciate all members in Redeemed Christian Postgraduate Fellowship, University of Ibadan (RCPGF, UI) and St. Mark’s Anglican Church, Ile-Ife for your prayers and spiritual support. Finally, I wish to thank my special friend Adedapo, Adedoyin Oluseyi whose steps have been ordered by God to share my vision and assist in achieving all. May God crown your efforts and perfect everything that concerns you in Jesus’ name. To God be the glory. v Certification I certify that this research work was carried out under my supervision by Ayodele Timilehin ADESOJI in the Department of Microbiology, Faculty of Science, University of Ibadan, Nigeria. ------------------------------------------------------------ Supervisor Dr. A. A. Ogunjobi B.Sc (OSUA), M.Sc, PhD (Ibadan) Department of Microbiology University of Ibadan, Ibadan, Nigeria vi Dedication To God Almighty and the entire family of Prof. and Mrs. F. A. Adesoji who God used to nurture me from childhood to who I am at present vii Abbreviations BLAST Basic Local Alignment Search Tool BOD Biochemical Oxygen Demand BSA Bovine Serum Albumin CLSI Clinical and Laboratory Standard Institute COD Chemical Oxygen Demand CS Conserved Segment DNA Deoxyribonucleic Acid EMB Eosine Methylene Blue FES Fetal Equine Serum LB Luria Bertani MDR Multi-drug Resistance PCR Polymerase Chain Reaction SA-HRP Streptavidin-Horseradish Peroxidase SDS Sodium dodecyl Sulphate SSC Saline Sodium Citrate TAE Tris-Acetic EDTA TBE Tris-Borate EDTA TDS Total Dissolved solid TNT Tris-Nacl Tween TOC Total Organic Carbon TS Total Solid TSA Tyramide Signal Amplification TSS Total Suspended Solid viii Table of Contents Subject Pages Title i Abstract ii Acknowledgements iv Certification vi Dedication vii Abbreviations viii Table of Contents ix List of Figures xvi List of Plates xvii List of Tables xviii Chapter 1 Introduction 1 1.1. Objectives of the study 5 Chapter 2 Literature Review 2.1. Dams construction and their uses 6 2.2. Water borne diseases 6 2.3. Environment and antibiotics 7 2.3.1. Antibiotics in the environment 7 2.3.2. Bacteria resistance in the environment 8 2.3.3. Sources of antibiotic resistance in the environment 9 2.3.3.1. Hospital wastewater 9 2.3.3.2. Surface water 9 2.3.3.3. Ground water 9 2.3.3.4. Drinking water 10 2.3.3.5. Sediments 10 ix Subject Pages 2.4. Mechanisms of antibiotic resistance 11 2.4.1. Genetic mechanism of transmission 12 2.4.1.1 Conjugation 12 2.4.1.2 Transformation 13 2.4.1.3. Transduction 13 2.4.2.0 Elements involved in horizontal transfer of resistance gene 14 2.4.2.1. Plasmid 14 2.4.2.2. Transposon 14 2.4.2.3. Integrons and gene cassettes 16 2.4.3. Biochemistry of Antibiotic resistance 18 2.4.3.1. Antibiotics inactivation 19 2.4.3.1.1 Antibiotics inactivation by hydrolysis 19 2.4.3.1.2. Antibiotics inactivation by group transfer 19 2.4.3.2. Target modification 20 2.4.3.2.1. Peptidoglycan structure alteration 21 2.4.3.2.2. Protein synthesis interference 21 2.4.3.2.3. DNA synthesis interference 22 2.4.3.3. Efflux pumps and outer membrane (OM) permeability 22 24 24 24 2.4.3.3.1.
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