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A Leap Towards Unravelling the Soil Microbiome

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A Leap Towards Unravelling the Soil Microbiome A leap towards unravelling the soil microbiome Paula Harkes Thesis committee Promotor Prof. Dr Jaap Bakker Professor of Nematology, Wageningen University & Research Co-promotor Dr Johannes Helder Associate Professor at the Laboratory of Nematology, Wageningen University & Research Other members Prof. Dr Wietse de Boer, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen Dr Davide Bulgarelli, University of Dundee, England Prof. Dr George Kowalchuk, Utrecht University Prof. Dr Franciska de Vries, University of Amsterdam This research was conducted under the auspices of the C.T. de Wit Graduate School of Production Ecology and Resource Conservation. A leap towards unravelling the soil microbiome Paula Harkes Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday 10 January 2020 at 4:00 p.m. in the Aula. Paula Harkes A leap towards unravelling the soil microbiome PhD Thesis Wageningen University, Wageningen, The Netherlands (2020) With references and with summaries in English and Dutch. ISBN: 978-94-6395-150-0 DOI: 10.18174/501980 “There's no limit to how much you'll know, depending how far beyond zebra you go.” Dr. Seuss ― Table of contents Chapter 1 General introduction 9 Chapter 2 The differential impact of a native and a non-native 23 ragwort species (Senecioneae) on the first and second trophic level of the rhizosphere food web Chapter 3 The habitat- and season-independent increase in fungal 55 biomass induced by the invasive giant goldenrod is asymmetrically reflected in the fungivorous nematode community Chapter 4 Mapping of long-term impact of conventional and organic 85 soil management on resident and active fractions of rhizosphere communities of barley Chapter 5 Organic management strengthens interkingdom 119 relationships in the soil and rhizosphere of barley Chapter 6 Mapping shifts in the active rhizobiome that might 155 underlie low Meloidogyne chitwoodi densities in fields under prolonged organic soil management Chapter 7 General discussion 189 Summary 204 Samenvatting 207 Acknowledgements 211 About the author 218 List of publications 219 PE&RC training and Education Statement 220 1 CHAPTER General introduction Paula Harkes Chapter 1 “The soil is the great connector of lives, the source and destination of all. It is the healer and restorer and resurrector, by which disease passes into health, age into youth, death into life. Without proper care for it we can have no community, because without proper care for it we can have no life.” Wendell Berry ― Soil: From Black box to Pandora’s box When you take a walk outside and your feet touch the ground, you may not realize that you are standing on the most densely populated habitat on earth. Soil houses an enormous quantity and diversity of organisms. More organisms live in one gram of soil than there are people on this planet. This crowded gram is inhabited by up to 10 billion bacteria, meters of fungal hyphae, and a wide variety of nematodes, earthworms, protists, and arthropods (Bardgett and van der Putten 2014; Raynaud and Nunan 2014). For a long time, people referred to soil as being a black box, as we were unable to characterize the exact life that was present in it. The main reason for this obliviousness is that only 1–5% of the soil bacterial population is culturable and this percentage is estimated to be even lower for fungi (Bakken 1997; Janssen et al. 2002; van Elsas et al. 2000). The diversity of soil life contributes substantially to the functioning of terrestrial ecosystems (e.g. nutrient cycling, promoting plant productivity, water holding capacity etc.) (Neher 1999). The identification of soil communities is therefore perceived as an important challenge by many scientists. With the introduction of DNA sequencing it became possible to identify the diversity of microbial communities. During the last decade, high-throughput sequencing has become less expensive and time consuming, making it currently the most frequently used technology in microbial ecology studies (Bartram et al. 2011; Fierer et al. 2012). Nowadays we can generate data in such a high turnover that the once described black box of soil – of which we did not know what it contained – can now be seen as Pandora’s box, as we are challenged to distil useful information from the immense data pile in order to comprehend the myriad of relationships and interactions that occur in soil. There’s always a bigger fish: The soil food web To visualize and better understand multidimensional relationships in soil, a soil food web approach can be used to link various trophic groups (Moore and de Ruiter 10 General introduction 2012). Most soil food webs distinguish four trophic levels (TLs) in which each level includes organisms that feed on dwellers of a preceding level (Fig. 1). Organic material from soil and plant roots form TL0 and are considered the primary producers. TL1 contains the organisms that feed directly on living plant materials (e.g. plant-parasitic 1 nematodes) and the primary decomposers that decompose organic substrates (i.e. bacteria and fungi). The second level (TL2) includes nematodes, protists and mites feeding on the primary decomposers. The highest level (TL3) are predacious organisms such as predatory mites, collembolans and nematodes. The composition of food webs is highly variable both in terms of space and time. Small changes in the biomass of particular organisms can have a marked, disproportionate and asymmetrical effect on soil processes (Berg and Bengtsson 2007). Therefore, in order to better understand soil community dynamics, it would be desirable to monitor all trophic levels at once. However, due to technical and financial restrains, the majority of studies concerning soil biodiversity and ecosystem functioning focus on either the primary decomposers or on indicator groups rep- The soil food web Roots Nematodes Protists Plant parasitic Arthropods Predatory Nematodes Bacterivorous Bacteria Protists Predatory Arthropods Shredders Organic matter Fungi Nematodes Nematodes Fungivorous Predatory TL 1 TL 2 TL 3 TL 4 Figure 1: An example of a soil food web in which trophic connections are indicated by arrows. Arrows are pointed towards their consumers. TL = Trophic Level. 11 Chapter 1 resented at different trophic levels – such as nematodes and earthworms (Griffiths et al. 2016). Even though soil microbes are the main players in nutrient cycling, focusing exclusively on the primary decomposers will preclude vital information, as the activity and biomass of bacteria and fungi is also affected by higher trophic levels (de Vries et al. 2013). For example, grazing mesofauna is able to enhance the rate of nutrient mineralization by 30% which, as a consequence, influences the productiv- ity of plants. This illustrates that it may be too much of a conjecture to link plant growth solitary to microbes (Gebremikael et al. 2016; Postma-Blaauw et al. 2010). Similar to studies centred on microbes, studies that concentrate solely on soil fauna can also be considered fragmentary in the context of improving our understanding of soil ecosystem functioning. For example, research on mesofauna has been mainly based on controlled greenhouse experiments, such as microcosms (Nielsen et al. 2011), and few studies have engaged on the effect of altered soil fauna community structure on processes across ecosystems (Sackett et al. 2010). Another limitation is the fact that indicator groups are often classified in trophic groups (e.g. bacterial feeders and fungal feeders). Although our insight in dietary preferences of nematodes is still fragmentary, research points at selective grazing (Hasna et al. 2007; Quist et al. 2014). Thereby making it more informative to investigate if particular changes in primary decomposer community are reflected in the next trophic level. In conclusion, a holistic approach to monitoring the soil food web, that includes multiple trophic levels measured at a high taxonomic resolution, can provide us with more information on interactions and changes in soil communities. The force awakens: Dormancy and activity in the rhizosphere Being present in the soil is not the same as actively participating in the soil food web. Soil is a particularly heterogeneous ecosystem (Van Elsas et al. 2006). Abiotic factors such as moist, nutrient availability and temperature fluctuate vastly, creating temporal and spatial variation. To cope with these capricious circumstances, microorganisms have the ability to reduce their metabolic activity over an extended period of time (Guppy and Withers 1999; Kaprelyants et al. 1993). This state of reduced activity is often referred to as ‘dormant’, although ‘quiescent’ is a more accurate term since it refers to reduced activity resulting from the influence of solely external factors (Rao 2018). The majority of soils are considered suboptimal for microbial growth, for instance because of lack of nutrients and/or energy sources, causing up to 80% of the cells to be dormant (Lennon and Jones 2011; Nannipieri et al. 2003). These 12 General introduction dormant communities, also referred to as microbial seedbanks, can be awakened when adequate environmental stimuli (e.g. organic substrates) are detected. Under such condition microbial hotspots can be formed (De Nobili et al. 2001). One important microbial hotspot is the rhizosphere; soil in the vicinity of plant roots, 1 in which large amounts of organic compounds are released by plants (Sanaullah et al. 2016). This process of rhizodeposition allows plants to specifically tune the activity, abundance and composition of the local microbial communities to their advantage (Brimecombe et al. 2007). In order to unravel which part of the microbial community is affected by a specific plant, it is important to distinguish between the active and total – also referred to as ‘resident’ – community. In combined community profiling, both the active and total fractions are analysed.
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