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University of Groningen the Ecology and Evolution of Bacteriophages Of University of Groningen The ecology and evolution of bacteriophages of mycosphere-inhabiting Paraburkholderia spp. Pratama, Akbar Adjie IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2018 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Pratama, A. A. (2018). The ecology and evolution of bacteriophages of mycosphere-inhabiting Paraburkholderia spp. Rijksuniversiteit Groningen. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 29-09-2021 Chapter 1 General Introduction Akbar Adjie Pratama and Jan Dirk van Elsas Partly published in Book chapter: The viruses in soil – potential roles, activities and impacts. Van Elsas J.D., Trevors J.T., Rosado A.S., and Nannipieri P., Taylor and Francis, 2018. Modern Soil Microbiology III. In press General introduction | Chapter 1 1 Essentially, all life depends upon the soil. There can be no life without soil and no soil without life; they have evolved together (Charles E. Kellogg) The living soil, soil activity hot spots and phages The living soil is a very heterogeneous and dynamic system that influences microbial contact, attachment, niche differentiation and diversity. Its heterogeneity stems from the diversity of soil physicochemical characteristics and soil environmental conditions (e.g. pH, salinity) that have shaped both macro- and microhabitats across soil space and time (Fierer, 2017). The most dynamic activity in soil can be observed in microhabitats that are nutrient-rich and have been denominated hotspots. The factors that affect the life in soil hotspots include soil density, redox potential and nutrient contents, the latter spurring dynamically active and diverse microbiomes. Key known activity hotspots in the living soil are (i) the rhizosphere, i.e. the soil volume surrounding living roots; (ii) the detritusphere, i.e. organic litter that may consist of plant and/or animal residues, (iii) biopores, i.e. the soil surrounding animal-caused burrows (mainly earthworms), also known as the drillosphere. Other biopores such as the termitosphere (burrow caused by termites) and myrmecosphere (burrow caused by ants) should also be noted, yet the extent to which these affect microbial dynamics is understudied. (iv) aggregate surfaces, i.e. hotspots formed as the consequence of the movement of dissolved organic matter (DOM) through soil pores. Finally (v), the mycosphere, i.e. the region surrounding fungal hypae in soil (for details, see Zhang et al., 2014) stands out as a highly relevant yet hitherto understudied soil activity hot spot. All hotspots are ecologically significant for the functioning of the soil (e.g. decomposition, mineralization as well as build-up of soil organic matter). In generic terms, they increase microbial processes and interactions and consequently accelerate microbial exchange pools and evolution. With respect to the mycosphere, we may safely state that it is a highly dynamic microhabitat in terms of local conditions that are shaped by the microbially-mediated as well as physicochemical processes that shift over time. This is discussed further in the next section. The dynamic conditions are thought to shape the lifestyle of mycosphere inhabitants. 11 Chapter 1 | General introduction In general, soil microbiomes include bacteria, fungi, archaea, protozoa, as well as their respective viruses. Compared to bacteria, the study of soil viruses is still in its infancy. Adding up to it, the role of soil viruses as shapers of the ecology and the evolution of soil microbiomes is still poorly understood, as compared to marine counterparts. In the study reported in this thesis, I focus on the importance of soil viruses, especially bacteriophages, for the ecology and evolution of mycosphere inhabitants. The phage like or related genes in there lay the basis of this thesis. The importance of horizontal gene transfer (HGT) in soil is undoubtedly great, as evidenced by major studies on soil-derived bacteria. I conclude this introduction by developing concepts on the roles of phages in mycosphere dwellers, which yield hypotheses underlying the work described in each of the chapters. The mycosphere in soil and the key mycosphere inhabitant Paraburkholderia terrae In soil microbiomes, bacteria are often dominant, both in terms of numbers, diversity and activity. Their diversity across soil space and time is immense and has been well documented (Torsvik et al., 1990). Moreover, their role in global ecological processes such as degradation, mineralization and fixation processes is essential. Next to bacteria, fungi also (i) are abundant with respect to cell numbers (expressed as hyphal length), and (ii) play significant roles in soil functioning. Some of the fundamental questions with respect to the ecology of soil microbial communities are therefore: how are bacterial-fungal interactions (BFI) established? What are the key players and roles in these interactions? What are the molecular/ecological mechanisms behind it? And, what are the consequences of such interactions for the ecosystem functions in soil and the benefits between the partners. The mycosphere is known to provide carbonaceous compounds that are released by fungal cells, including oxalate, glycerol, formate, acetate, fumarate, mannitol, trehalose, erythritol, arabitol, citric acid and amino acids (Boersma et al., 2010; Frey, 1997; Haq et al 2018). These offer ecological opportunities to soil bacteria that are able to utilize, and thrive on, these released compounds. Here, I briefly describe the system used in this study, the mycosphere inhabitant Paraburkholderia terrae interacting with host fungi in the soil. It was found this organism has intricate strategies to interact with soil fungi (Haq et al., 2014; Nazir et al., 2012; Warmink et al., 2011; Yang et al., 2016). P. terrae has been shown to have “high-affinity” fungal-interactive behavior, with the ectomycorrhizal fungus Laccaria proxima in soil under hazel trees (see Figure 1.1). Thus, assessments based on culture-dependent (isolation and colony-plate counting) and culture-independent 12 General introduction | Chapter 1 assays (molecular detection of a type-3 secretion system (T3SS) proxy, the hrcC gene) for three consecutive years on L. proxima mycospheres showed significant increases 1 of P. terrae (exemplified by strain BS110), as compared to the corresponding bulk soil. This suggested the occurrence of positive selection of these organisms presumably by the nutrients released by the fungi (Warmink and van Elsas, 2008). Further studies in soil microcosms revealed a strong profiency of another P. terrae strain, denoted BS001, for migration along the growing hyphae of the soil saprotroph Lyophyllum strain Karsten. This fungal-interactive behavior possibly involved a complex array of mechanisms, including motility, the T3SS and biofilm formation, which was observed surrounding the fungi hyphae (Warmink and Van Elsas, 2009). Strain BS001 was indeed a proficient single-strain migrator along the growing hyphae, next to P. terrae strains BS007, BS110, DSM 17804T and P. hospita DSM 17164T (Nazir et al., 2012). The mechanisms behind the interaction of P. terrae with soil fungi have also been addressed extensively (Haq et al., 2014, 2016, 2017, Yang et al., 2016, 2017, 2018). The involvement of the T3SS was investigated by comparing the knock-out strain P. terrae sctD with the wild-type strain, as regards its growth, nutrient utilization ability and migration profiency. No significant differences were observed in terms of BS001Δ growth, nutrient utilization (BIOLOG GEN III plates assay) and migratory ability in single inoculation experiments. However, mixed (1:1 ratio) inoculation experiments showed the wild-type to outcompete the mutant. Thus the T3SS possibly played a subtle role in the comigration along fungal hyphae, helping P. terrae in attachment to the host cell surface. Interestingly, this behaviour was shown with both L. sp. strain Karsten and Trichoderma asperellum 302 (Yang et al., 2016). The ability of P. terrae to adhere to fungal cell walls was then investigated (using ELISA), with a focus on the glycosphingolipids ceramide monohexosides (CMHs) that possibly play roles in fungal cell envelopes. The results showed adherence of the P. terrae wild-type to CMH of L. sp. strain Karsen but not to that of T. asperellum 302 and to a lesser extent of the sctD mutant. Subsequently, addition of P. terrae BS001 enhanced the total biomass with L. sp. strain Karsten but not with T. asperellum 302 (Haq et al., 2016). Δ fliP pliN) revealed the essential role of functional flagella for migration along with fungal hyphae, next to a minor Work with a flagellar mutant (Δ ) and a T4P one (Δ positive effect of the T4P. In conclusion, the migration of P. terrae BS001 along fungal hyphae was posited to be a strongly flagellar-driven process (Yang et al., 2017). The movement of P. terrae strain BS001 towards the fungal-released compounds glycerol and oxalic acid has also been addressed (Haq et al., 2016, 2018). Both compounds indeed promoted the movement of the cells.
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