On the Ecology and Evolution of Microorganisms Associated with Fungus-Growing Termites
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On the ecology and evolution of microorganisms associated with fungus-growing termites Anna A. Visser Propositions 1 Showing the occurrence of a certain organism in a mutualistic symbiosis does not prove a specific role of this organism for that mutualism, as is illustrated by Actinobacteria species occurring in fungus-growing termite nests. (this thesis) 2 Instead of playing a role as mutualistic symbiont, Pseudoxylaria behaves like a weed, competing for the fungus-comb substrate and forcing termites to do regular gardening lest it overgrows their Termitomyces monoculture. (this thesis) 3 Citing colleagues who are no longer active must be considered as an act of true altruism. 4 The overload of literature on recent ‘discoveries’ blinds us from old literature, causing researchers to neglect what was already known and possibly duplicate investigations. 5 Keys to evolution of knowledge lie in recognizing the truth of one’s intuition, and extending the limits of one’s imagination. 6 The presumed creative superiority of left-handed people (Newland 1981), said to be the result of more communication between both sides of the brain, might rather be the result of lifelong selection on finding creative solutions to survive in a right-hand biased environment. 7 An understanding of ‘why good ideas usually come by the time time is running out and how to manage this’, would greatly improve people’s intellectual output and the condition in which they perform. Propositions accompanying the thesis “On the ecology and evolution of microorganisms associated with fungus-growing termites” Anna A. Visser Wageningen, 15th June 2011 Reference Newland GA, 1981. Differences between left and right-handers on a measure of creativity. Perceptual and Motor Skills 53: 787-792.Stellingen Stellingen 1. Het aantonen van de aanwezigheid van een bepaald organisme in een mutualistische symbiose bewijst niet dat dit organisme een specifieke rol speelt in die mutualistische symbiose, zoals wordt geïllustreerd door Actinobacteriën die in nesten van schimmelkwekende termieten voorkomen. (dit proefschrift) 2. Pseudoxylaria gedraagt zich niet als een mutualistische symbiont maar als een onkruid, concurrerend om het substraat van de schimmeltuin en de termieten dwingend tot regelmatig tuinieren – zo niet dan overwoekert ze de Termitomyces monocultuur. (dit proefschrift) 3. Het citeren van collegae die niet meer actief zijn moet worden opgevat als een daad van werkelijk altruïsme. 4. De overmaat aan literatuur over recente ‘ontdekkingen’ maakt ons blind voor oude literatuur, wat als gevolg heeft dat onderzoekers negeren wat al bekend was en mogelijk onderzoek herhalen. 5. De sleutel tot evolutie van kennis ligt in het herkennen van de waarheid in iemands intuïtie, en het verleggen van de grenzen van iemands voorstellingsvermogen. 6. De veronderstelde creatieve superioriteit van linkshandige mensen (Newland 1981), naar zeggen het resultaat van meer communicatie tussen de beide hersenhelften, zou eerder het resultaat kunnen zijn van levenslange selectie op het vinden van creatieve oplossingen om in een rechtshandig georiënteerde omgeving te overleven. 7. Begrip van ‘waarom goede ideeën meestal komen tegen de tijd dat tijd schaars wordt en hoe dit te reguleren’, zou de intellectuele prestatie van mensen en de staat waarin ze presteren aanzienlijk kunnen verbeteren. Stellingen behorende bij het proefschrift getiteld “On the ecology and evolution of microorganisms associated with fungus-growing termites” Anna A. Visser Wageningen, 15 Juni 2011 Referentie Newland GA, 1981. Differences between left and right-handers on a measure of creativity. Perceptual and Motor Skills 53: 787-792. Thesis committee Thesis supervisors Prof. dr. R. F. Hoekstra Emeritus professor of Genetics (Population and Quantitative Genetics) Prof. dr. T. W. Kuyper Personal Chair at the department of Soil Quality, Wageningen University Thesis c0-supervisors Dr. D. K. Aanen Assistant professor at the Laboratory of Genetics, Wageningen University Dr. ir. A. J. M. Debets Associate professor at the Laboratory of Genetics, Wageningen University Other members Prof. dr. P. W. Crous, Wageningen University Prof. dr. A. van Huis, Wageningen University Dr. E. T. Kiers, VU University, Amsterdam Prof. dr. J. I. Korb, University of Osnabrück, Germany This research was conducted under the auspices of the C. T. De Wit Graduate School of Production Ecology & Resource Conservation (PE&RC). Anna Alida Visser On the ecology and evolution of microorganisms associated with fungus-growing termites Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Wednesday 15 June 2011 at 11 a.m. in the Aula. Anna A. Visser (2011) On the ecology and evolution of microorganisms associated with fungus-growing termites PhD Thesis, Wageningen University, Wageningen, the Netherlands With references, with summaries in Dutch and English ISBN 978-90-8585-914-7 Contents Chapter 1 6 General Introduction: Termites, Engineering, and Fungiculture Chapter 2 26 Levels of specificity of Xylaria species associated with fungus- growing termites: a phylogenetic approach Chapter 3 54 Pseudoxylaria as stowaway of the fungus-growing termite nest: interaction asymmetry between Pseudoxylaria, Termitomyces and free-living relatives Chapter 4 80 The role of termite workers in controlling Pseudoxylaria and other fungi in their fungus garden Chapter 5 102 Actinobacteria from fungus-growing termites lack specificity for host and target: an unlikely defence against Pseudoxylaria despite antibiotic potential Chapter 6 140 General Discussion: Termite Fungiculture Revisited Summary 162 Samenvatting 166 Affiliation of co-authors 170 Acknowledgements 171 Curriculum Vitae 173 PE&RC PhD Education Certificate 174 Chapter 1 - General Introduction: Termites, Engineering, and Fungiculture “The termites resemble the ants also in their provident and diligent labour, but surpass them as well as the bees, wasps, beavers, and all other animals which I have ever heard of, in the arts of building. It [Macrotermes bellicosus] erects immense buildings of well-tempered earth, which are contrived and finished with such art and ingenuity, that we are at a loss to say, whether they are most to be admired on that account, or for their enormous magnitude and solidity.” – Smeathman 1781 – Termites (Insecta, order Blattodea) dominate and shape the landscape in large parts of the world (Batra & Batra 1979; Abe et al. 2009), and in doing so they are often referred to as ecosystem engineers. The tunnels they dig during mound-building and foraging make the soil permeable for water and air (Konaté et al. 1999). Additionally, termites are of chief importance for their contribution to organic matter turnover. They play a crucial part in turning dead plant matter into minerals (Lepage 1984; Jones 1990; Mando & Brussaard 1999; Abe et al. 2009), breaking down a quarter of the yearly primary production that is not consumed by fire (Kuyper 2004). With the scale on which they affect physical and chemical soil properties (Mando & Miedema 1997; Jouquet et al. 2005), termites are crucial for soil quality. Nutrient-rich patches around termite mounds affect the landscape by offering favourable conditions for plant seedlings to survive (Kiepe 1984; Jouquet et al. 2005), creating clusters of vegetation that are better known as ‘islands of fertility’ (Levick et al. 2010; Sileshi et al. 2010), see also Figure 1-1. Indisputably, termites play a paramount role in a range of ecosystems. For that reason termites are considered ‘ecosystem engineers’ (Pardeshi & Prusty 2010). Of an estimated total of four-thousand termite species 2,500 have been described. Nearly 2,000 of these belong to the family Termitidae. This family contains a subfamily that has adopted an exceptional lifestyle: agriculture (or rather fungiculture). The 6 General Introduction: Termites, Engineering, and Fungiculture Figure 1-1 Impression of islands of fertility. Aerial picture of Kenyan landscape with clusters of trees (dark spots with a diameter of ± fifteen meters). ©Google Earth 2010 Macrotermitinae (11 genera, about 330 species; Kambhampati & Eggleton 2000) no longer depend solely on the microbiota in their gut for digestion of plant matter, but they cultivate a fungus that digests the substrate outside their body (Sands 1969; Batra & Batra 1979; Wood & Thomas 1989; Darlington 1994). As illustrated in Figure 1-2, the termites collect and comminute dead plant material that they then deposit in the nest as hardly digested faeces. These faecal deposits are piled up to form a sponge-shaped structure that is overgrown by Termitomyces and named ‘fungus comb’ (Sands 1960). Enhanced by the warm, moist and stable climate of the termite mound, Termitomyces degrades the plant material and produces nodules (primordial fruiting bodies). The nodules – nitrogen-rich and high-quality food compared to the original, often woody, plant material – are eaten by the termites and act as inocula of newly added comb substrate (Sands 1960; Batra 1975; Sieber & Leuthold 1981). Finally, also the digested parts of the fungus comb substrate are consumed by the termites, resulting in final faeces which are deposited outside the nest (Darlington 1994). This cooperation between termite and fungus has made them incredibly successful and allowed them to dominate the landscape