Spill your guts: the invasive amphibian gut microbiome

Wagener, Carla (2021-03)

Thesis (MSc)--Stellenbosch University, 2021.

Thesis

ENGLISH ABSTRACT: Invasive vertebrate species threaten global biodiversity, and significantly impact economic, agricultural and ecosystem services. Alarmingly, the number of introductions of species into non-native areas are increasing. Invasive species are introduced along with non-native microorganisms living in or on their hosts. In plant and insect invasions it has been shown that symbiotic relationships with microbial communities (collectively known as the microbiome) can enhance invasive species performance and facilitate establishment of non-native species in new environments. However, no studies have determined which factors impact the invasive vertebrate microbiome and how different microbial communities might facilitate vertebrate invasions. Therefore, in the aim of this thesis was to study how introduction of a vertebrate species into novel environments alters it’s gut microbial communities and it’s predicted functional capabilities, as well as whether the gut microbiome and it’s functional profiles can respond adaptively to environmental change and how these responses (or lack thereof) affect host physiology and, ultimately, fitness. To address the first aim outlined above, I made use of next-generation DNA sequencing (NGS) techniques to characterise the gut bacterial communities of guttural toad (Sclerophrys gutturalis) invasive populations in Mauritius, Réunion and Cape Town with varying residence times and compared these to their native source population in Durban. This allowed me to test whether residence time impacts the gut microbial compositional, phylogenetic and functional divergence across guttural toad populations. Additionally, I characterised the gut microbiome of an expanding invasive population (Cape Town) to determine how residence time impacts gut microbial divergence across the core and periphery. To address my second aim, I conducted reciprocal faecal microbial transplant experiments on native and invasive guttural toads in Durban (native area) and Cape Town (invasive area). Thereafter I exposed toads to one of two diets: natural or a dietary challenge and subsequently collected faecal microbial material in order to determine compositional, phylogenetic and functional microbial responses of toads to a novel dietary challenge. Additionally, I measured physiological performance and organ mass of toads. I found that gut microbial communities are compositionally distinct across all invasive populations. However, only the youngest population had a phylogenetic and functionally distinct microbiome. Therefore, I found that residence time does not impact the gut microbiomes of invasive guttural toads and instead I suggest that invasion pathways (i.e. the life history of toads at introduction) might be a more important factor determining gut microbiome divergence. I found that the invasive Cape Town microbiome has adaptively diverged to become compositionally, phylogenetically and functionally flexible in response to a novel dietary challenge compared to the native Durban microbiome. Functional pathways known to increase digestive efficiency, additionally increased in abundance in the invasive microbiome. I also found that this microbial flexibility facilitates flexibility in energy investments in hosts. Although physiological performance did not vary across diets, performance was significantly higher in toads with invasive gut microbiomes. Thus, I show for the first time that the gut microbiome facilitates ecological adaptation in an invasive amphibian population.

AFRIKAANSE OPSOMMING: Indringer werwel spesies bedreig natuurlike biodiversiteit regoor die wêreld en het ‘n beduidende impak op ekonomiese, lanbou- en ekosisteem dienste. Die aantal spesies wat van hulle natuurlike habitat beweeg word na uitheemse omgewings is aan die toeneem. Indringer spesies bring saam met hulle mikro-organismes wat in of op hulle gashere lewe. Altesaam word alle mikro-organismes word verwys na die mikrobioom. Vir plant en insek indringer spesies is voordelige verhoudings met die mikrobioom uiters belangrik vir die gasheer se fisiologie en kan suksesvolle vesting van indringer spesies in uithemese omgewings fasiliteer. Geen studies het al ooit ondersoek of die werweldier mikrobioom die gasheer se indringer potensiaal kan verbeter nie. Dus was die doel van hierdie proefskrif om te bestudeer watse faktore die derm mikrobioom en sy funksionele vermoëns impak wanneer ‘n indringer werweldier, die gorrelskurwe padda (Sclerophrys gutturalis), beweeg word van ‘n natuurlike omgewing na ‘n uithemese omgewing. Boonop het hierdie proefskrif ondersoek of die indringer derm mikrobioom kan aanpas na ‘n dieetuitdaging in vergelyking met die natuurlike, inheemse derm mikrobioom en of enige verandering in die derm mikroboom veranderinge sal aanbring in die fisiologie van die paddas. Om die bogenoemde doelwitte aan te spreek, het ek gebruik gemaak van volgende generasie DNA-basis volgorde bepalings tegnieke om die derm bakteriële gemeenskappe van paddas in Mauritius, Réunion en Kaapstad met wisselende verblyf tye te kenmerk en vergelyk aan hulle inheemse bronbevolking in Durban, Suid Afrika. Dit het my in staat gestel om te toets of verblyftyd die mikrobiese samestelling, filogenetiese en funksionele diversiteit beïnvloed van hierdie padda bevolkings. Verder het ek die derm mikrobioom van ‘n uitbreidende bevolking gekarakteriseer om vas te stel of verblyftyd die mikrobioom beïnvloed van ‘n groeiende bevolking by sy kern en periferie. Om my tweede doelwit te bereik het ek wederkerige mikrobiese fekale oorplantings op inheemse en uitheemse paddas in Durban (inheemse omgewing) en Kaapstad (uitheemse omgewing) voltooi. Daarna het ek paddas bloodgestel aan een van twee diete; ‘n natuurlike dieet of ‘n dieetuitdaging. Aan die einde van die eksperimente het ek die fekale mikrobiese materiaal van paddas versamel om die samestelling, filogenetiese en funksionele mikrobioom reaksies op die dieetuitdaging te bepaal. Verder het ek die uithouvermoë en energie berging van paddas bepaal. Die derm mikrobioom samestelling is uniek in alle beveolkings van die gorrelskurwe padda. Alhoewel, net die jongste populasie het ‘n filogenetiese en funksioneel unieke derm mikrobioom. Dus, het ek gevind dat verblyftyd nie die derm mikrobioom van hierdie paddas beïnvloed nie. Ek stel voor dat indringsweë (dit wil sê die lewens siklus gedurende beweging van indringer spesies) ‘n kern faktor is wat die derm mikrobioom van hierdie padda beïnvloed. Verder vind ek dat die Kaapstadse mikrobioom aangepas is om te reageer op omgewings verandering terwyl die inheemse, Durban, mikrobioom nie reageer wanneer paddas na ‘n dieetsuitdaging blootgestel word nie. Ek vind dat die mikrobioom fasiliteer die vermoë van paddas om energie te stoor en langer afstande en ‘n hoër spoed bereik wanner hulle spring. Ek wys dus vir die eerste keer dat die werweldier mikrobioom nie net kan aanpas tot ‘n nuwe ompegewing nie maar dat die mikrobioom die fisiologie van die gasheer reguleer.

Please refer to this item in SUNScholar by using the following persistent URL: http://hdl.handle.net/10019.1/110075
This item appears in the following collections: