The influence of mitochondrial inhibitors on zoospore and ascospore development

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Date
2010-11
Authors
Swart, Chantel W.
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University of the Free State
Abstract
English: In 2007, Kock and co-workers published the Acetylsalicylic acid (ASA) Antifungal Hypothesis that indicated a definite link between oxylipin production [3-hydroxy (OH) oxylipins], mitochondrial activity [mitochondrial transmembrane potential (Δψm)] and ASA sensitivity in respiring as well as non-respiring yeasts. Here an increase in mitochondrial activity was observed in the sexual phase where an increase in energy production is probably needed for multiple ascospore development. This hypothesis has since been expanded to also include various anti-mitochondrial drugs as well as the fungi and fungi-like organisms Aspergillus, Rhizopus and Mucor. In this study the yeast Nadsonia fulvescens as well as some species of the notorious plant pathogen Phytophthora was evaluated for their ability to fit the expanded hypothesis now called the Anti-mitochondrial Antifungal Hypothesis. The yeast N. fulvescens is characterized by a unique life cycle. After conjugation between the parent cell and the first bud, the zygote moves into a second bud formed at the opposite end of the parent cell. This second bud is then delimited by a septum and becomes the ascus according to literature. Usually one, rarely two spherical, brownish, spiny to warty ascospores are formed within the ascus giving rise to brown coloured colonies. In this study the parent cell with attached first bud showed increased mitochondrial activity when compared to the ascus. When anti-mitochondrial compounds were added, the mitochondrial activity was inhibited in the parent cell with attached first bud followed by the formation of less asci with ascospores (many not fully developed and white coloured). It is suggested that sufficient mitochondrial activity in the parent cell and first bud is necessary to produce enough energy for the formation of a proper ascus with brown coloured ascospore(s). If the parent cell and first bud is regarded as part of the yeast sexual phase, then N. fulvescens also fits the hypothesis. Further investigations were conducted to study the asci of the yeast N. fulvescens containing mature and fluconazole-treated malformed ascospores using nano scanning Auger microscopy (NanoSAM) in combination with transmission electron microscopy (TEM). This is the first application of NanoSAM to biological material. Transmission electron microscopy exposed a variety of malformed ascospores in asci treated with fluconazole. Here some ascospores produced degenerated spiky protuberances with relatively large inclusions carried inside wrinkled asci. Other ascospores contained no walls or protuberances and were enclosed within smooth spherical shaped asci. The majority of ascospores contained less dense hollow areas surrounded by cytoplasmic material. Nano scanning Auger microscopy studies on these asci corroborate the TEM results although less structural detail was obtained. Nano scanning Auger microscopy showed a decrease in elemental intensities during etching which assisted structural analysis of ascospore less dense hollow areas. In this study it is shown that the oomycete, Phytophthora nicotianae also fits the hypothesis. Fruiting structures (zoosporangia) of this oomycete showed increased beta (β)-oxidation when probing levels of 3-OH oxylipins with specific polyclonal antibodies. In addition increased mitochondrial activity was also observed in the zoosporangia when the Δψm probe, Rhodamine 123 was added to the culture. This indicates increased mitochondrial activity in the zoosporangia when compared to the hyphae. When the anti-mitochondrial ASA was added to cultures of this oomycete, the zoosporangia were, as expected most susceptible and were drastically inhibited in the presence of 1 mM of this compound. Similar ASA inhibition results were recorded for P. citrophthora. Anti-mitochondrial compounds may now find application in combating these devastating plant pathogens and urgent further research is needed in this direction.
Afrikaans: In 2007 publiseer Kock en mede-werkers die Asetielsalisielsuur (ASS) Antifungale Hipotese wat „n definitiewe verband voorstel tussen oksilipienproduksie [3-hidroksie (OH) oksilipiene], mitochondriale aktiwiteit [mitochondriale transmembraan potensiaal (Δψm)] en ASS sensitiwiteit in respirerende sowel as nie-respirerende giste. Tydens die bogenoemde studie is „n toename in mitochondriale aktiwiteit waargeneem in die geslagtelike (seksuele) fase waar „n toename in energie produksie moontlik nodig is vir die vorming van veelvoudige askospore. Hierdie hipotese is sedertdien uitgebrei om verskeie anti-mitochondriale middels asook fungi en fungi-agtige organismes soos byvoorbeeld Aspergillus, Rhizopus en Mucor in te sluit. In hierdie studie is die gis Nadsonia fulvescens sowel as sekere spesies van die bekende plant patogeen Phytophthora getoets vir hul vermoë om in te pas by die uitgebreide hipotese, nou genoem die Anti-mitochondriale Antifungale Hipotese. Die gis N. fulvescens word gekarakteriseer deur „n unieke lewenssiklus. Na konjugasie tussen die moedersel en die eerste botsel, beweeg die sigoot na „n tweede botsel wat vorm aan die teenoorgestelde kant van die moedersel. Hierdie tweede botsel word afgesper deur „n septum en vorm die askus volgens literatuur. Gewoonlik word een, in rare gevalle twee, bruin, stekelagtige tot vratagtige askospore gevorm binne die askus wat lei tot die vorming van bruin kolonies. In hierdie studie toon die moedersel met aangehegde eerste botsel „n verhoging in mitochondriale aktiwiteit in vergelyking met die askus. Byvoeging van anti-mitochondriale middels het die mitochondriale aktiwiteit in die moedersel met eerste botsel ge-inhibeer, gevolg deur die vorming van minder aski met askospore (baie nie volledig ontwikkeld nie en wit in kleur). Daar word voorgestel dat verhoogde mitochondriale aktiwiteit nodig is in die moedersel en eerste botsel om genoeg energie te produseer vir die vorming van volwasse aski met bruin gekleurde askospore. Indien die moedersel tesame met die eerste botsel beskou word as deel van die gis se geslagtelike voortplantingsfase, dan pas N. fulvescens in die hipotese. Verdere studies is ook gedoen om die aski van die gis N. fulvescens met volwasse en fluconazole-behandelde askospore te bestudeer met nano skanderings Auger-mikroskopie (NanoSAM) in kombinasie met transmissie-elektronmikroskopie (TEM). Hierdie is die eerste toepassing van NanoSAM op biologiese materiaal. Transmissie-elektronmikroskopie het „n verskeidenheid van misvormde askospore in aski wat behandel is met fluconazole ontbloot. Sommige askospore het misvormde stekelagtige uitsteeksels getoon met relatief groot insluitsels in die geplooide askus. Ander askospore het geen wande of uitsteeksels gehad nie en is waargeneem in gladde, sferiese aski. Die meerderheid askospore het minder digte areas bevat, wat omring word deur sitoplasmiese materiaal. Nano skanderings Auger-mikroskopie studies op hierdie aski stem ooreen met die TEM resultate alhoewel minder strukturele besonderhede waargeneem is. Nano skanderings Auger-mikroskopie het „n afname in element intensiteit ontbloot tydens etsing wat gehelp het met die strukturele analise van die minder digte areas in die aski. In die studie is ook aangetoon dat die oomiseet, Phytophthora nicotianae wel inpas by die hipotese. Vrugliggame (zoosporangia) van hierdie oomiseet het „n toename in beta (β)-oksidasie getoon met „n merker vir 3-OH oksilipiene (spesifieke poliklonale teenliggame). Verder is verhoogde mitochondriale aktiwiteit waargeneem in die zoosporangia wanneer die Δψm merker, Rhodamien 123 by die kultuur gevoeg is. Dit wys daarop dat daar verhoogde aktiwiteit in die zoosporangia voorkom wanneer dit vergelyk word met vegetatiewe hifes. Wanneer die anti-mitochondriale middel ASS by kulture van hierdie oomiseet gevoeg is, is bevind dat die zoosporangia meer sensitief is as die hifes. „n Aansienlike vermindering in zoosporangium vorming is waargeneem in die teenwoordigheid van 1 mM ASS. Soortgelyke ASS-inhibisie studie resultate is waargeneem vir P. citrophthora. Anti-mitochondriale middels kan moontlik nou aangewend word om hierdie plant patogene te bekamp en dringende verdere studies is nodig in hierdie verband.
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Keywords
Mycoses -- Treatment, Medical mycology, Ascospores, Mitochondria, Transmission electron microscopy, Thesis (Ph.D. (Microbial, Biochemical and Food Biotechnology))--University of the Free State, 2010, Asci, Elemental composition, Fluconazole, Life cycle, Mitochondrial inhibitors, Nadsonia fulvescens, Nano scanning Auger microscopy, Phytophthora, Plant pathogen, Sexual phase, 3-dimensional architecture
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