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THE BIOLOGY and RESPIRATORY PHYSIOLOGY of APHELENCHUS AVENAE BASTIAN 1B65 by Aruna Hemalkantha Wilfred Mendis B.Sc. Hons, [Sri L

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THE BIOLOGY and RESPIRATORY PHYSIOLOGY of APHELENCHUS AVENAE BASTIAN 1B65 by Aruna Hemalkantha Wilfred Mendis B.Sc. Hons, [Sri L THE BIOLOGY AND RESPIRATORY PHYSIOLOGY OF APHELENCHUS AVENAE BASTIAN 1B65 by Aruna Hemalkantha Wilfred Mendis B.Sc. Hons, [Sri Lanka], DIC [London} M.Sc. [London] The -thesis submitted for the degree of Doctor of Philosophy in the Faculty of Science, University of London Department of Zoology and Applied Entomology Imperial College of Science and Technology Silwood Park, Ashurst Lodge, Ascot Berkshire June 1981 i ACKNOWLEDGEMENTS I gratefully acknowledge the love, encouragement and financial help given me by my parents - Alfric and Sita CAmmi] Mendis - and my parents-in-law - Joe and Laurine Perera - without which this work would not have been possible. I would like to thank Profassor T.R.E. Southwood, F.R.S., and Professor M.J. Way for giving me the opportunity to work at the Silwood Park Field Station. I am indebted to Dr. Adrian A.F. Evans for sparking my interest in nematode physiology with characteristic. enthusiasm, and for his continual interest, encouragement and excellent supervision of my project. I also thank him for nominating me for and the British Council for presenting me with an Overseas Students Fees Award. I would like to take this opportunity to thank several people, namely, Dr. Dennis J. Wright and Dr. D.P. Mcmanus for their advice, Or. John M. Palmer for allowing me the use of the Amino Chance spectrophotometer and for his valuable advice, Dr. J. Crawley and Dr. Stephen Young for advice on statistics and Dr. Kay S. Cheah for his advice and useful comments on the results of this study, I would also like to thank Mrs. V. Bennett for her excellent typing of the script and her sense of humour even under duress. Special thanks to my cousin Carmeline Perera for the generous loan of the typewriter. I wish to thank my wife Anne-marie For her financial and moral support and useful criticism of the script. Finally, I would like to thank my son Jehann For providing the "diversion" - required or otherwise - without which this thesis may have seen the binder much earlier. dedicate "this thesis my wife and son iii Abstract Three isolates of Aphelenchus avenae were mass cultured monoxenically and assessed for bio- physiological variation. Isolates E and F [From U.K.3 reproduced parthenogenetically; Isolate A [From Malawi] reproduced amphimicticly. The oxygen consump- tion rates [QOgD of all three isolates were similar but declined with time of harvest. Arrhenius plots of the QOg data [Log QOg vs. 1/ K] showed "intersecting" type discontinuities at different temperatures depend- ing on isolate. Isolates differed also in population development rates at 10°C to 30°C. Arrhenius plots i.e. Log population development rate vs. 1/°K, corresponded very closely with those obtained with the QOg data and probably indicates the occurrence of "thermotypes" within the species. Each isolate differed in response of the QOg of the whole worms [cultured at 25°CD to 3 mM NaCN. The QOg of isolate-F was 75-80% inhibited, Q0g of isolate-E was 0-12% inhibited and that of isolate-A was 17-20% inhibited. The QOg of isolate-A cultured at 30°C was stimulated by 3 mM NaCN. When cultured at 25°C, stimulation of the QOg was observed only following prolonged incubation at 30°C. iv Mitochondrial fractions of isolates A and F utilised only succinate and 06-glycerophosphate to any significant extent. The respiratory control ratios [RCRs] were higher for isolate-F as were the PsO ratios. Antimycin-A had little or no effect on the state-3 QOg of isolate-A but caused near complete inhibition of the state-3 QOg of Isolate-F. The ascorbate-TMPD-oxidase activity of isolate-A was only partially [55-65%] inhibited by 3 mM NaCN while that of isolate-F was completely inhibited. Salicylhydroxamic acid [SHAM] produced 50-60% inhibition of the residual [=cyanide insensitive] QOg of isolate-A [i.e. 20-30% of total QOg] but carbon monoxide [CO] was required for complete inhibition. Spectrophotometric observations showed the presence of cytochromes b, c and a in mitochondrial fractions of all isolates. Treatment with CO altered the spectra considerably giving almost identical spectra to those described for Moniezla expansa and Halobacterium sps. as .characteristic of cyt.O. A. avenae probably has three potentially functional terminal oxidases, cyt. aa^; cyt. 0 and possibly an OC-glycerol-phosphate-oxidase [GPO]. The latter complex linked to glycolysis, may be responsible for the production of glycerol detected in isolates A and F by 6LC techniques. CONTENTS Page ACKNOWLEDGEMENTS i ABSTRACT iii CHAPTER 1 - General Introduction 1 CHAPTER 2 - General Materials and Methods 16 CHAPTER 3 - Biological variation among three isolates of Aphelenchus avenae Introduction 21 Materials and Methods 27 Results 34 Discussion 44 CHAPTER 4 - The effect of Physical factors on the respiratory physiology of three isolates of A. avenae Introduction 52 Materials and Methods 69 Results 52 Oiscussion 66 CHAPTER 5 - The effect of chemical agents on the respiratory oxygen consumption of A. avenae isolates A, F and E Introduction 73 Materials and Methods 77 Results 88 Discussion 1Q2 CHAPTER 6 - Analysis of metabolic end-products secreted by whole-worms of A»avenae isolates A and F Introduction 118 Materials and Methods 122 . Results 124 Discussion 126 Pago CHAPTER 7 - Studios on the mitochondrial Fractions of A> avenae isolates A and F Introduction 131 CHAPTER 7A - Investigation of the oxidative capacities of the mitochondrial Fractions of A. avenae isolates A and F Materials and Methods 149 Results 154 Discussion 160 CHAPTER 7B - Spectrophotometric analysis of cytochromes in the mitochondrial preparations of isolates A and F Materials and Methods 175 Results 183 Discussion 196 CHAPTER 8 - Final Discussion 217 BIBLIOGRAPHY 230 APPENDICES 245 CHAPTER 1 General Introduction The electron transfer sequences in parasites has been suggested to depart from the classical- mammalian pattern. CBryant, 1970; Barrett, 1976} The main source of difference» according to Bryant [1970D, involves the suppression of an oxygen-dependent terminal oxidase in favour of one or more alternative pathways capable of utilizing different electron acceptors resulting in the development of branched electron transport sequences. Whether this difference is directly related to the parasitic habit is one of the more interesting questions helminthologists and protozoologists are attempting to clarify, although Barrett C1976] has suggested that the importance of oxidative processes in the overall energy balance of helminths differ in different parasites and may even vary between tissues of the same parasite. Therefore in order to provide an adequate answer to this,a more complete understanding of parasite metabolism might be obtained by reference to the most closely related free-living forms with which they are presumed to have shared a common ancestor. Although a comprehensive literature has accumulated on the respiratory-electron transport systems as obtains in parasitic helminths such as Moniezia expansa, Ascaris and Fasciola, there is relatively little literature on the respiratory-characteristics of free living nematodes. However^ spectra obtained from homogenates' of a fresh-water turbellarian Cura pinguis CBryant S Fletcher as quoted by Bryant 1970], and the free-living gt.alo nematodes Caenorhabditis briggsae CBryantf 19673 and Turbatrix aceti CRothstein et al_- ,19703 were reported to be similar to spectra obtained with M. expansa preparations * CBryant, 19703 suggesting that the branched system may be more widely distributed in nature. On this basis Bryant C19703 suggested that the relationship between the branched respiratory chain and parasitism is not direct, and that groups of organisms which became successful parasites possessed these modifications because they were already adapted to conditions which bore certain resemblances to the parasitic environments. Fundamentally the intestines are special cases of a whole class of environments in which oxygen tension or the amount of available oxygen is low. CBryant, 1970 3 The soil environment with its variety of texture, fluctuating oxygen tension, pH and humidity may well have been the habitat that offered the greatest challenge to the archetypal land-based freeliving nematode, acting as an important evolutionary "spring-board" for the parasitic habit. For this reason it is logically the best habitat in which to seek the predecessors of the parasitic mode. If the extent of geographical distribution is any measure of evolutionary success, Aphelenchus avenae with its cosmopolitan distribution, its wide host range and 3 short generation time, would be an ideal model to employ in order to study and gain an insight into the metabolic processes [respiratory or otherwise] associated with parasitic nematode species. However the same attributes that make A. avenae a model organism For such studies may present some difficulties. For instance, geographically separated populations [or isolates] may have adapted to specific local conditions and therefore different isolates may not be homogeneous in their physio-biochemical response to an externally applied physical or chemical constraint[s]. Indeed since the monoxenic cultures of A. avenae may be harvested at any time between 30 and 140 days, a considerable variation in response may be expected even within a single isolate. In this respect the data on the oxygen consumption rates [QOg] of whole worms of A. avenae differ consider- ably according to figures cited by various authors. Cooper [1969] and Cooper and Van Gundy C1970a] quoted a figure of 5.6-5.8 yl Og/mg dry wt./hour at 28°C; Marks [1971] quoted a rate of 10-12 ^jl Og/mg dry wt./ hour at 30°C; Awan [1975] obt ained a mean rate between 4.64 and 4.89 ^il Og/mg dry wt./hour. Although these workers apparently employed different strains of A. avenae they however did not report the age of the cultures from which these populations were derived. Preliminary investigations into the variation of the Q0p of mixed stages of one isolate of A.
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