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Symbiosis Between the Cyanobacterium Nostoc and the Liverwort Blasia Requires a Cher-Type MCP Methyltransferase

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Symbiosis Between the Cyanobacterium Nostoc and the Liverwort Blasia Requires a Cher-Type MCP Methyltransferase Symbiosis between the cyanobacterium Nostoc and the liverwort Blasia requires a CheR-type MCP methyltransferase Paula S. Duggan, Teresa Thiel & David G. Adams Symbiosis ISSN 0334-5114 Volume 59 Number 2 Symbiosis (2013) 59:111-120 DOI 10.1007/s13199-012-0216-9 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Symbiosis (2013) 59:111–120 DOI 10.1007/s13199-012-0216-9 Symbiosis between the cyanobacterium Nostoc and the liverwort Blasia requires a CheR-type MCP methyltransferase Paula S. Duggan & Teresa Thiel & David G. Adams Received: 24 October 2012 /Accepted: 10 December 2012 /Published online: 29 December 2012 # Springer Science+Business Media Dordrecht 2012 Abstract In response to environmental change, the cyanobac- and hornworts (Adams et al. 2012; Adams and Duggan 2008, terium Nostoc punctiforme ATCC 29133 produces highly 2011; Bergman et al. 2008). In response to certain environmen- adapted filaments known as hormogonia that have gliding tal stimuli Nostoc develops small-celled, motile filaments motility and serve as the agents of infection in symbioses with known as hormogonia, which are essential for infection of the plants. Hormogonia sense and respond to unidentified plant- host plant (reviewed by Bergman et al. 2007; Meeks and Elhai derived chemical signals that attract and guide them towards 2002;Meeks2009; Adams and Duggan 2011). Indeed, host the symbiotic tissues of the host. There is increasing evidence plants release hormogonium-inducing factors (Bergman et al. to suggest that their interaction with host plants is regulated by 1996; Campbell and Meeks 1989; Cohen and Meeks 1997; chemotaxis-related signal transduction systems. The genome Knight and Adams 1996; Rasmussen et al. 1994; Watts et al. of N. punctiforme contains multiple sets of chemotaxis (che)- 1999). Hormogonia formation involves the up-regulation of like genes. In this study we characterize the large che5 locus of 944 genes, the majority of which appear to be involved in N. punctiforme. Disruption of NpR0248, which encodes a signal transduction and transcriptional activation (Campbell et putative CheR methyltransferase, results in loss of motility al. 2007). The hormogonium is therefore highly adapted to and significantly impairs symbiotic competency with the liver- sense and respond rapidly to its environment and is specialised wort Blasia pusilla when compared with the parent strain. Our for motility, dispersal and the initiation of symbiosis with host results suggest that chemotaxis-like elements regulate hormo- plants (e.g. Adams and Duggan 2008; Bergman et al. 2008; gonia function and hence symbiotic competency in this system. Meeks 2009). The surface of Nostoc punctiforme hormogonia is covered with pili (fimbriae) that are important for the infec- Keywords Symbiosis . Cyanobacteria . Nostoc . Liverwort tion process and may be involved in motility, host recognition and surface attachment (Duggan et al. 2007). Work in our laboratory (Knight and Adams 1996; Watts 1 Introduction et al. 1999) as well as by others (Nilsson et al. 2006; see also Adams and Duggan 2011) has shown that plant-derived Filamentous cyanobacteria of the genus Nostoc form symbiotic signals likely act as chemoattractants, guiding hormogonia associations with a wide range of plants, including liverworts towards the sites of infection within the host plant. However, the molecular elements regulating this process have yet to be characterised. One of the best studied che- P. S. Duggan : D. G. Adams Institute of Integrative and Comparative Biology, Faculty of motaxis systems is the regulation of flagellar-based motility Biological Sciences, University of Leeds, Leeds LS2 9JT, UK in Escherichia coli (Sourjik 2004; Wadhams and Armitage 2004). Transmembrane chemoreceptors (MCPs, methyl- T. Thiel accepting chemotaxis proteins) perceive extracellular stim- Department of Biology, University of Missouri-St. Louis, St. Louis, MO 63121, USA uli, producing signals that are transmitted to their cytoplas- mic domains. These domains regulate an associated two- D. G. Adams (*) component phosphotransfer signal transduction system, Institute of Integrative and Comparative Biology, CheA-CheY (with a linker protein CheW) that controls Garstang Building, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK flagellar rotation by binding to the flagellar motor protein e-mail: [email protected] FliM. Additional components of the chemotaxis machinery Author's personal copy 112 P.S. Duggan et al. include CheB, a methylesterase, and CheR, a methyltrans- Collection, PCC 73102; a kind gift of Jack Meeks) was orig- ferase, that modulate the methylation status of MCPs, which inally isolated from a symbiotic association with the cycad affects their sensitivity. CheB, activated through phosphor- Macrozamia (Rippka et al. 1979). N. punctiforme and its ylation of CheA, removes the methyl groups added to MCPs derivatives were grown in BG11 medium (which contains by CheR, leading to an adaptive response that enables the 17.5 mM NaNO3 as combined nitrogen source; Rippka et al. bacterium to respond to new stimuli in a background contain- 1979) with shaking at 27 °C with continuous irradiance of ing constant levels of chemoattractants and/or repellents (Bren 23 μmolm−2s−1. Recombinant N. punctiforme 29133 were and Eisenbach 2000; Clausznitzer et al. 2010). Chemotaxis- selected for resistance to, and maintained in, the presence of like genes are widespread among bacteria, and many are 25 μgml−1 neomycin (Nm). E. coli strains DH5α (plasmid known to be involved in signalling pathways that regulate construction) and HB101 (conjugation experiments) were rou- functions distinct from their well established role in the regu- tinely grown in Luria-Bertani medium (Sambrook et al. 1989) lation of chemotaxis (reviewed by Kirby 2009). Some exam- supplemented, as appropriate, with antibiotics, ampicillin (Ap; ples include the regulation of pili gene expression in the 100 μgml−1), kanamycin (Km 50 μgml−1) and chloramphen- unicellular cyanobacterium Synechocystis sp. PCC 6803 icol (Cm; 170 μgml−1). The liverwort Blasia pusilla was (Bhaya et al. 2001; Chung et al. 2001), virulence gene expres- growninliquidBG11mediumwithshakingat100rpm,at sion in Vibrio cholerae (Lee et al. 2001), biofilm formation 20 °C under a 12 h/12 h light/dark cycle (average light irradi- (Tran et al. 2008; see also Kirby 2009), fibril biogenesis and ance of 20 μmolm−2s−1). expression of developmental genes in Myxococcus xanthus (Yang et al. 2000; Kirby and Zusman 2003). Red light induction of hormogonia formation N. puncti- N. punctiforme hormogonia exhibit both chemotactic and forme filaments recovered by centrifugation were washed phototactic behaviour. Directed motility likely requires a signal three times in BG110 medium (BG11 lacking combined transduction system to detect the appropriate attractant in the nitrogen) and resuspended in twice the original culture environment and communicate the information to a motility volume of BG110. Flasks were covered with red cellophane apparatus. In the N. punctiforme genome sequence (completed and incubated for 18 h at 27 °C with shaking and a contin- by the Joint Genome Institute and available at http://www.jgi. uous irradiance of 50 μmolm−2s−1 to allow hormogonia to doe.gov; Meeks et al. 2001)therearefiveloci(designatedche1- develop. 5) containing ORFs exhibiting sequence similarity to known chemotaxis (che) genes from other bacterial species. Unlike the Reconstitution of symbiotic associations Nitrogen starved other loci, the che5 locus, containing seven che-like ORFs (by growing for 10–14 days in BG110) B. pusilla tissue (NpR0244-NpR0250),appearstohavebeenacquiredbyhori- (2–2.5 cm2 in diameter and 0.8–0.85 g wet wt) was co- zontal gene transfer (Wuichet and Zhulin 2003). This locus cultured with mutant and wild-type N. punctiforme (at a lacks the cheY-like genes found in the other 4 loci, but contains total chlorophyll a content of 100 μg) as described previ- genes encoding a response regulator receiver modulated CheB ously (Duggan et al. 2007). In the Blasia symbiosis the methylesterase (NpR0244) and a tetratricopeptide repeat cyanobacteria occupy dome-shaped structures known as (TPR)-containing CheR-type MCP methyltransferase auricles on the surface of the thallus. The number of sym- (NpR0248). The TPR domain is a structural motif found in a biotic colonies (i.e. infected auricles) was determined mi- wide range of proteins and mediates protein-protein interactions croscopically after 14 and 28 days of co-culture and the (Blatch and Lassle 1999). Genes encoding two other CheR frequency of infection expressed as a percentage of the total proteins and three additional CheB-like proteins have been number of auricles counted (at least 400 auricles were found elsewhere in the N. punctiforme genome. The additional counted for each determination). CheB proteins may have different physiological roles as they lack the response regulator receiver domain that is receptive
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