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Mycophagous Soil Bacteria

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Mycophagous Soil Bacteria MYCOPHAGOUS SOIL BACTERIA MAX-BERNHARD RUDNICK Thesis committee Promotor Prof. Dr Wietse de Boer Professor of Microbial Soil Ecology Wageningen University Co-promotor Prof. Dr Hans van Veen Professor of Microbial Ecology Leiden University Other members Prof. Dr Kornelia Smalla, Technical University Braunschweig, Germany Prof. Dr Michael Bonkowski, Cologne University, Germany Prof. Dr Joana Falcão Salles, Groningen University Prof. Dr Hauke Smidt, Wageningen University This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology & Resource Conservation (PE&RC) MYCOPHAGOUS SOIL BACTERIA MAX-BERNHARD RUDNICK 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 Friday 13th of February 2015 at 1.30 p.m. in the Aula. Max-Bernhard Rudnick Mycophagous soil bacteria 161 pages. PhD thesis, Wageningen University, Wageningen, NL (2015) With references, with summaries in Dutch and English. ISBN: 978-94-6257-253-9 “Imagination is more important than knowledge” - Albert Einstein - - A l b e r t E i n s t e i n - TABLE OF CONTENTS ABSTRACT 9 INTRODUCTION COLLIMONADS AND OTHER MYCOPHAGOUS SOIL BACTERIA 11 CHAPTER TWO OXALIC ACID: A SIGNAL MOLECULE FOR FUNGUS-FEEDING BACTERIA OF THE GENUS COLLIMONAS? 21 CHAPTER THREE EARLY COLONIZERS OF NEW HABITATS REPRESENT A MINORITY OF THE SOIL BACTERIAL COMMUNITY 35 CHAPTER FOUR TRAIT DIFFERENTIATION AMONG MYCOPHAGOUS COLLIMONAS BACTERIA 51 CHAPTER FIVE A SAPROTROPHIC EXTENSION OF THE MYCORRHIZOSPHERE: MYCOPHAGOUS RHIZOBACTERIA RECOVERED FROM FUNGUS INCUBATION-BAITING ASSAYS 87 CHAPTER SIX BAITING AND ENRICHING FUNGUS FEEDING (MYCOPHAGOUS) BACTERIA 111 CHAPTER SEVEN GENERAL DISCUSSION 127 REFERENCES 137 SUMMARY 151 SAMENVATTING 153 ACKNOWLEDGEMENTS 155 CURRICULUM VITAE 159 COLLIMONADS AND OTHER MYCOPHAGOUS BACTERIA IN THE RHIZOSPHERE ABSTRACT Soil microorganisms evolved several strategies to compete for limited nutrients in soil. Bacteria of the genus Collimonas developed a way to exploit fungi as a source of organic nutrients. This strategy has been termed “mycophagy”. In this thesis, research is presented with a focus on two aspects of bacterial mycophagy: 1) Investigation of strategies and traits that are important for Collimonas bacteria to enable a mycophagous lifestyle, 2) Investigation of occurrence of mycophagy among other soil bacteria. Focusing on Collimonas bacteria, we find that several traits related to the mycophagous interaction with the fungal hosts, such as production of fungal inhibitors, are phylogenetically conserved. This implies that differentiation in lifestyles of Collimonas strains, is corresponding with phylogenetic distance. Furthermore, we show that collimonads are very motile in a soil- like matrix, especially when being confronted with low nutrient concentrations. This high motility can be used in order to effectively move towards oxalic acid (a metabolite exuded by a range of fungi for different purposes) in a concentration depended manner. Our results suggest that directed motility is an important trait, characterizing the mycophagous lifestyle of collimonads. In order to screen for other mycophagous bacteria besides collimonads, two baiting approaches (long- and short-term) were developed. With both approaches, we find fungal hyphae to be commonly colonized by specific communities of rhizosphere mycophagous bacteria. Furthermore, mycophagous colonizers show clear feeding preferences for fungal hosts. Interestingly, a surprisingly high amount of mycophagous bacteria belong to genera well known to harbor plant pathogenic strains. Considering the importance of mycophagous bacteria in the rhizosphere, we finally propose the “Sapro-Rhizosphere” concept. This concept states that a substantial amount of plant derived carbon that is channeled through rhizosphere fungi (primary consumers) might be finally consumed by mycophagous bacteria (secondary consumers). Taken together, by using molecular biological as well as microbiological methods, this thesis further extends our knowledge on the ecology of mycophagous Collimonas bacteria and highlights the importance of mycophagous bacteria in the rhizosphere. 9 COLLIMONADS AND OTHER MYCOPHAGOUS BACTERIA IN THE RHIZOSPHERE INTRODUCTION COLLIMONADS AND OTHER MYCOPHAGOUS BACTERIA 11 INTRODUCTION MICROBIAL SOIL ECOLOGY Soil is a very complex and heterogeneous environment. Abiotic factors like pH, moisture and physical characteristics vary substantially between soils and can also rapidly change locally, thus creating a variety of possibilities for survival and growth of microbial species with different niches. It has been argued that the high number of potential microbial habitats is a major contributor to below-ground microbial species diversity, ranging from 103-107 different OTUs (Operational Taxonomical Units) per 10g of soil (Schloss & Handelsman 2006; Roesch et al. 2007; Timonen & Bomberg 2009; Uroz et al. 2010). The microscopic heterogeneity of soil with different pore sizes, distribution of water films and gradients of organic and inorganic nutrients, offers potential for microbial niche adaptation. Since soil microstructure and environmental conditions vary a lot with fluctuations in soil pH, water content and temperature gradients, adaption to different soil habitats is a frequent mechanism in the evolutionary shaping of soil microbial communities (Crawford et al. 2005). Microorganisms fulfill a variety of functions in soil. They are capable of catalyzing all steps in soil nutrient cycling, being responsible for mineralization and decomposition for example. Breakdown of easily accessible compounds is mainly performed by bacteria that are able to exert quick growth when nutrient conditions are optimal. Saprotrophic fungi are the dominant microorganisms when it comes to degradation of recalcitrant substances like the plant secondary structural cell wall component lignin (de Boer et al. 2005). Fungi and bacteria colonize new soil habitats in different ways. Microbial dispersal in soil is strongly controlled by soil moisture. Low moisture content leads to less connectivity between water filled soil pores. This restricts passive (diffusion) and active bacterial movement (flagella), finally influencing bacterial abilities to colonize new microhabitats (Vos et al. 2013). Fungi grow with prolongation of their hyphal system, and are therefore able to bypass air filled soil pores. It has also been shown that bacteria are able to move along fungal hyphae in order to cross these air filled gaps (Kohlmeier et al. 2005). THE RHIZOSPHERE AND ITS INHABITANTS Despite the fact that soils offer an immense amount of microhabitats, the majority of the accessible internal soil surfaces and pores are deserted because of a lack of nutrients. In fact, the vegetated first centimeters of the soil is the place where most microbial life concentrates. Plants release carbon via exudation through their roots, thus creating an oasis for microbial soil life around their roots, a zone called the rhizosphere. Here, most of the interactions between different microorganisms, and also between microorganisms and higher organisms (e.g. plants or nematodes) occur. In the following lines I want to focus on interactions between plants and their direct microbial environment, descriptions of interactions of other higher organisms with microorganisms can be found elsewhere (Bonkowski 2004; Davies 2005; Zientz et al. 2005; Curry & Schmidt 2006; Kaneda & Kaneko 2008). Plant roots interact via exudates with the surrounding microbes (Bais et al. 2006; de Boer et al. 2006; Haichar et al. 2008; Bonfante & Anca 2009; Buee et al. 2009; Dennis et al. 2010; Uroz et al. 2010). Different plant species harbor a microbial community that is well distinguishable and steered by species-specific root exudate composition (Berg & Smalla 2009). Root exudation is in turn affected by the biotic and abiotic environment and by plant developmental stage 12 COLLIMONADS AND OTHER MYCOPHAGOUS BACTERIA IN THE RHIZOSPHERE (Hartmann et al. 2009; Bezemer et al. 2010; Uroz et al. 2010; Chaparro et al. 2013; Chaparro et al. 2014). By providing a generally carbon-limited environment with easily accessible energy sources plants attract a diverse community of bacteria and fungi which developed various strategies to acquire plant derived organic nutrients. One of those strategies is to invade the plant root. Some bacteria and fungi manage to overcome or modify the physical and chemical plant defenses, enabling them to internally colonize the plant root and other organs. These endophytes avoid competition in the rhizosphere by completely living inside the host or by physically “tapping” the source even before it releases nutrients into the rhizosphere. Some endophytes establish a connection with the plant root, but still extend into the rhizosphere with most of their tissue. The mycorrhizal fungi for example colonize the plant root internally but still extend far into the rhizosphere. Those endophytic fungi do not only take carbon from the plant host, they also provide the plant with “goods” such as phosphorus, thus creating a situation with benefits for both partners. Other, parasitic or pathogenic fungi like Rhizoctonia solani e.g. colonize the plant root and cause diseases with detrimental effects for plant performance. FUNGAL-BACTERIAL INTERACTIONS IN THE
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