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Type VI Secretion Systems of Plant‐Pathogenic Burkholderia Glumae BGR1 Play a Functionally Distinct Role in Interspecies Inter

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Type VI Secretion Systems of Plant‐Pathogenic Burkholderia Glumae BGR1 Play a Functionally Distinct Role in Interspecies Inter Received: 21 April 2020 | Revised: 28 May 2020 | Accepted: 31 May 2020 DOI: 10.1111/mpp.12966 ORIGINAL ARTICLE Type VI secretion systems of plant-pathogenic Burkholderia glumae BGR1 play a functionally distinct role in interspecies interactions and virulence Namgyu Kim1 | Jin Ju Kim2 | Inyoung Kim1 | Mohamed Mannaa1 | Jungwook Park1 | Juyun Kim1 | Hyun-Hee Lee1 | Sais-Beul Lee3 | Dong-Soo Park3 | Woo Jun Sul2 | Young-Su Seo 1 1Department of Integrated Biological Science, Pusan National University, Busan, Abstract Korea In the environment, bacteria show close association, such as interspecies interaction, 2 Department of Systems Biotechnology, with other bacteria as well as host organisms. The type VI secretion system (T6SS) Chung-Ang University, Anseong, Korea 3National Institute of Crop Science, Milyang, in gram-negative bacteria is involved in bacterial competition or virulence. The plant Korea pathogen Burkholderia glumae BGR1, causing bacterial panicle blight in rice, has four Correspondence T6SS gene clusters. The presence of at least one T6SS gene cluster in an organism Young-Su Seo, Department of Microbiology, indicates its distinct role, like in the bacterial and eukaryotic cell targeting system. In Pusan National University, Busan 609-735, Korea. this study, deletion mutants targeting four tssD genes, which encode the main com- Email: [email protected] ponent of T6SS needle formation, were constructed to functionally dissect the four Funding information T6SSs in B. glumae BGR1. We found that both T6SS group_4 and group_5, belonging the Strategic Initiative for Microbiomes to the eukaryotic targeting system, act independently as bacterial virulence factors in Agriculture and Food, Ministry of Agriculture, Food and Rural Affairs, toward host plants. In contrast, T6SS group_1 is involved in bacterial competition by Republic of Korea, Grant/Award Number: exerting antibacterial effects. The ΔtssD1 mutant lost the antibacterial effect of T6SS 918019-04; National Research Foundation of Korea, Grant/Award Number: NRF- group_1. The ΔtssD1 mutant showed similar virulence as the wild-type BGR1 in rice 2019R1A2C2006779 because the ΔtssD1 mutant, like the wild-type BGR1, still has key virulence factors such as toxin production towards rice. However, metagenomic analysis showed dif- ferent bacterial communities in rice infected with the ΔtssD1 mutant compared to wild-type BGR1. In particular, the T6SS group_1 controls endophytic plant-associated bacteria such as Luteibacter and Dyella in rice plants and may have an advantage in competing with endophytic plant-associated bacteria for settlement inside rice plants in the environment. Thus, B. glumae BGR1 causes disease using T6SSs with function- ally distinct roles. KEYWORDS bacterial competition, bacterial virulence, Burkholderia glumae, interspecies interaction, metagenomic analysis, TssD, type VI secretion system This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd Molecular Plant Pathology. 2020;21:1055–1069. wileyonlinelibrary.com/journal/mpp | 1055 1056 | KIM ET AL. 1 | INTRODUCTION co-regulated protein), and VgrG (valine-glycine repeat protein G) have been considered the hallmark apparatus of T6SS as well as secreted Myriad bacteria demonstrate close associations with nearby bacteria, effectors in all bacteria with functional T6SSs (Pukatzki et al., 2007). as well as with their host organisms (Freestone, 2013; Stubbendieck B. glumae is a gram-negative bacterium known as a seedborne et al., 2016). Bacteria can persist and adapt in their ecological niche phytopathogenic bacterium that causes bacterial panicle blight as by continuously interacting with other organisms, and have devel- well as sheath and seedling rot in rice (Oryza sativa) (Goto, 1956; Goto oped many protective and infectious mechanisms against competi- et al., 1987). The major virulence factors of B. glumae are toxoflavin, tors and host organisms. Some of these, such as bacterial secretion lipase, type III effectors, and extracellular polysaccharides, along systems, biofilms, and phytotoxins, provide survival benefits against with cell motility (Iiyama et al., 1995; Suzuki et al., 2004; Kim et al., bacterial and eukaryotic cells, and facilitate environmental adap- 2007; Kang et al., 2008; Lee et al., 2016; Jung et al., 2018). The T6SS tation (Backert and Meyer, 2006). In particular, bacterial secretion was classified into six groups based on the distribution of 5 out of 13 systems are considered the primary and effective means for com- T6SS components in 12 Burkholderia strains, including B. glumae (Seo munication and adaption to the surroundings (Russell et al., 2014). et al., 2015). Of these six T6SS groups, four T6SS groups are found in Bacterial secretion systems are classified into nine groups (Tat B. glumae BGR1. However, their functions are still unexplored. system, types I–VII, type IX) according to their structures, functions, In this study, we report that T6SS group_1 has antibacterial ef- and specific effectors (Stanley et al., 2000; Whitney et al., 2013; fects but is dispensable for virulence, whereas T6SS group_4 and Kneuper et al., 2014; Green and Mecsas, 2016). The type VI secre- T6SS group_5 were found to directly affect the pathogenicity of tion system (T6SS) was identified as a bacterial secretion system in B. glumae BGR1 targeting rice plants through phylogenetic analysis an opportunistic pathogen, Pseudomonas aeruginosa (Mougous et al., and a phenotypic assay. Furthermore, metagenomics analysis of the 2006). The T6SS is widespread in around 25% of gram-negative bac- endophytic bacterial community inside plants identified different teria and is easily found in pathogenic or symbiotic plant-associated bacterial communities with the ΔtssD1 mutant compared to those bacteria (Boyer et al., 2009; Bernal et al., 2018). The T6SS forms with the wild-type BGR1. This indicates that T6SS group_1 inhibits proteinaceous machinery that delivers substrates (effectors) to ad- or limits the growth of endophytic plant-associated bacteria, thereby jacent bacterial or eukaryotic cells in a contact-dependent manner helping pathogenic bacteria form a bacterial community easily. Our or releases effectors tothe extracellular environment. The effectors findings clearly describe the important role of T6SS in interspecies secreted by these systems are used to destroy and manipulate eu- interactions, including pathogen–host interaction and interaction karyotic cells and/or to fight other bacteria to gain dominant sta- with other bacteria. tus in the same ecological niche (Ma and Mekalanos, 2010). At least one T6SS gene cluster is present in some bacteria. The presence of two T6SS gene clusters in one organism increases the possibility 2 | RESULTS that each system has a different function depending on the circum- stances (Bingle et al., 2008). More recently, functional T6SSs were 2.1 | Evolutionary analysis of type VI secretion discovered in a broad spectrum of bacterial species and were found systems in Burkholderia species shows functional to contribute to virulence in host organisms, improve bacterial ro- differentiation based on environmental adaptation bustness, and enhance adaptation to polymicrobial environments through bacterial competition (Russell et al., 2014). For example, The evolutionary analysis of Burkholderia T6SS in B. mallei, B. pseu- P. aeruginosa has H1-T6SS, H2-T6SS, and H3-T6SS. H1-T6SS contrib- domallei, B. thailandensis, and B. cepacia, as well as in six rice-patho- utes only to interactions between bacteria by the delivery of toxins genic strains of B. plantarii, B. gladioli, and B. glumae, was performed and effector molecules (Hood et al., 2010). H2-T6SS and H3-T6SS to identify the distinct roles of the four T6SS in B. glumae BGR1, also exhibit antibacterial activity by secreting trans-kingdom effec- using at least 10 major core components of T6SS. The T6SS gene tors, but are involved in virulence against eukaryotes (Russell et al., clusters of B. glumae BGR1, B. plantarii ATCC43733, and B. gladioli 2013; Jiang et al., 2014). T6SS-5 of Burkholderia thailandensis is also BSR3 were annotated in our previous study (Seo et al., 2015). All a major virulence factor in the murine model of acute melioidosis Burkholderia species have at least one T6SS gene cluster. However, (Schwarz et al., 2010). we found that not all T6SS gene clusters of Burkholderia species were The T6SS is composed of a minimal set of 13 core components, completely composed of 13 major elements. In the resulting phylog- TssA–TssM (type six secretion). Apart from these major components, eny, six rice-pathogenic Burkholderia species were highly conserved several accessory proteins are encoded in the T6SS gene cluster, and in at least one T6SS gene cluster, which includes T6SS group_1 of work together with the T6SS effector to damage the inner membrane B. glumae, B. gladioli, and B. plantarii (Figure S1). These T6SS gene of prokaryotic target cells or participate in negative regulation of the clusters are closely clustered with B. thailandensis E264 T6SS-1, a T6SS (Miyata et al., 2013; Lin et al., 2018). These components are well-known bacterial cell targeting system (Schwarz et al., 2010). In generally encoded by clustered genes; each cluster has a different
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