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Vertical Transmission Explains the Specific Burkholderia Pattern In ORIGINAL RESEARCH ARTICLE published: 18 December 2013 doi: 10.3389/fmicb.2013.00394 Vertical transmission explains the specific Burkholderia pattern in Sphagnum mosses at multi-geographic scale Anastasia Bragina 1, Massimiliano Cardinale 1,2, Christian Berg 2 and Gabriele Berg 1* 1 Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria 2 Institute of Plant Sciences, Karl-Franzens University of Graz, Graz, Austria Edited by: The betaproteobacterial genus Burkholderia is known for its versatile interactions with Michael Schloter, Helmholtz its hosts that can range from beneficial to pathogenic. A plant-beneficial-environmental Zentrum München, Germany (PBE) Burkholderia cluster was recently separated from the pathogen cluster, yet still Reviewed by: little is known about burkholderial diversity, distribution, colonization, and transmission David J. Studholme, University of Exeter, UK patterns on plants. In our study, we applied a combination of high-throughput molecular Michael Schmid, Helmholtz Zentrum and microscopic methods to examine the aforementioned factors for Burkholderia München, Germany communities associated with Sphagnum mosses – model plants for long-term *Correspondence: associations – in Austrian and Russian bogs. Analysis of 16S rRNA gene amplicons Gabriele Berg, Institute of libraries revealed that most of the Burkholderia are part of the PBE group, but Environmental Biotechnology, Graz University of Technology, a minor fraction was closely related to B. glathei and B. andropogonis from the Petersgasse 10-12/I, Graz, 8010, pathogen cluster. Notably, Burkholderia showed highly similar composition patterns for Austria each moss species independent of the geographic region, and Burkholderia-specific e-mail: [email protected] fluorescent in situ hybridization of Sphagnum gametophytes exhibited similar colonization patterns in different Sphagnum species at multi-geographic scales. To explain these patterns, we compared the compositions of the surrounding water, gametophyte-, and sporophyte-associated microbiome at genus level and discovered that Burkholderia were present in the Sphagnum sporophyte and gametophyte, but were absent in the flark water. Therefore, Burkholderia is a part of the core microbiome transmitted from the moss sporophyte to the gametophyte. This suggests a vertical transmission of Burkholderia strains, and thus underlines their importance for the plants themselves. Keywords: Sphagnum fallax, Sphagnum magellanicum, Burkholderia communities, amplicon pyrosequencing, FISH-CLSM INTRODUCTION of them are characterized by an endophytic lifestyle (Sessitsch The genus Burkholderia, which was described by Yabuuchi et al. et al., 2005; Gasser et al., 2009; Mitter et al., 2013). While sin- (1992), encompasses a diverse group of Betaproteobacteria with gle strains of the PBE cluster are already well-characterized, currently more than 60 validly described species. Burkholderia little is known about the ecology and colonization pattern of species are known for their beneficial as well as pathogenic Burkholderia species on plants. interaction with plants, animals, and humans (Coenye and Plantshavebeenrecognizedasmeta-organismsduetotheir Vandamme, 2003). In the past, most studies focused on the close symbiotic relationship with their microbiome that fulfills pathogenic species for their enormous clinical importance important host functions (Berg, 2009; Bulgarelli et al., 2012; (Mahenthiralingam et al., 2005). Recently, a specific plant- Hirsch and Mauchline, 2012; Lundberg et al., 2012; Berg et al., beneficial-environmental (PBE) Burkholderia cluster that con- 2013). These advances were driven by both “omic”-technologies tains non-pathogenic species was divided from the cluster that guided by next-generation sequencing (NGS) and microscopic comprises human, animal and plant pathogens (Caballero- insights (Berendsen et al., 2012; Jansson et al., 2012). Mosses Mellado et al., 2007; Suárez-Moreno et al., 2010, 2012). However, belong to the phylogenetically oldest group of land plants on there is no clear border between both groups especially within the Earth, and their long-term intense relationship with their asso- plant-associated species; for example B. glathei was suggested to ciated microbes has contributed to the co-evolution of a highly be transfered from the pathogenic to the PBE group (Verstraete specific microbiome (Opelt and Berg, 2004; Opelt et al., 2007c; et al., 2013). Many PBE members belong to Burkholderia species Bragina et al., 2012). Therefore, mosses are important mod- symbiotic to tropical plants; each nodulating plant species is col- els in studying plant-microbe interactions and the ecology of onized by a single unique endophytic Burkholderia species (Van plant-associated bacteria. The genus Sphagnum is among the Oevelen et al., 2002; Lemaire et al., 2011). Several species from the most abundant and cosmopolitan of bog vegetation in the PBE cluster share characteristics that are of use in association with Northern hemisphere, and greatly contributes to both global car- plants, such as quorum sensing systems, the presence of nitro- bon turnover and global climate (Raghoebarsing et al., 2005; gen fixation and/or nodulation genes, and the ability to degrade Dise, 2009). The ecological significance of bogs is directly related aromatic compounds (Suárez-Moreno et al., 2012), and many to the physical, morphological, and chemical characteristics of www.frontiersin.org December 2013 | Volume 4 | Article 394 | 1 Bragina et al. Burkholderial diversity in Sphagnum Sphagnum peat mosses which set Sphagnum apart from other for isolation of the total-community DNA using the FastDNA® mosses in practically every stage of the life cycle (Daniels and SPIN Kit for Soil (MP Biomedicals, Solon, OH, USA). Final Eddy, 1985). Burkholderia species play an important role for aliquots of the total-community DNA were further used for a Sphagnum mosses and peatland ecosystem (Opelt et al., 2007a,b), deep sequencing-approach. and new Burkholderia species, which belong to the PBE clus- ter, have recently been isolated from these mosses (Vandamme 454-PYROSEQUENCING AND BIOINFORMATIC PROCESSING et al., 2007). However, their composition and occurrence on The diversity of the Sphagnum-associated microbiome with a Sphagnum at various geographical scales—ranging from the moss special focus on the genus Burkholderia was investigated using gametophyte and sporophyte up to continental level—is not yet a barcoded pyrosequencing technology. For this purpose, 16S understood. We hypothesize that Sphagnum species are colonized rDNA amplicons were generated using Taq-&Go™ Ready-to-use by specific Burkholderia from the PBE cluster independent from PCR Mix (MP Biomedicals, Solon, OH, USA). The total- the geographic region. community DNA of gametophyte samples was selectively ampli- To study this hypothesis and understand the ecological role, fied with Burkholderia-specific primers BKH143Fw/BKH1434Rw composition, colonization, as well as distribution pattern on (Schönmann et al., 2009) followed by amplification with uni- plants, we studied Burkholderia communities on two Sphagnum versal bacterial primers Unibac-II-515f/Unibac-II-927r (Lieber species (S. magellanicum and S. fallax) associated with different et al., 2003). In addition, the total-community DNA of S. fal- a-biotic parameters from different bogs in Austria and Russia. lax gametophyte samples from the bog Pürgschachen Moor We used an assortment of methods combining the analysis of (Table S1) and flark water sample was amplified with univer- Burkholderia-specific 16S rRNA gene pyrosequencing libraries sal bacterial primers Unibac-II-515f/Unibac-II-927r. The total- with FISH-CLSM analysis. Furthermore, we compared the com- community DNA of sporophyte samples was amplified with positions of water, gametophyte-, and sporophyte-associated universal bacterial primers 799f/1492r (Lane, 1991; Chelius and microbiomes to understand the transmission and distribution Triplett, 2001) because application of the Unibac-II-515f/Unibac- patterns of the Burkholderia communities. II-927r achieved mostly plant-derived sequences (data of pre- liminary experiments). Primer sequences are listed in Table 1. MATERIALS AND METHODS Duplicate PCR products from all templates were purified with SAMPLING DESIGN Wizard® SV Gel and PCR Clean-Up System (Promega, Madison, To analyze the diversity and distribution pattern of the WI, USA). Amplicons derived from the same Sphagnum sp. and Sphagnum-associated Burkholderia community, S. magellanicum sampling site were pooled in equimolar ratios and subjected to BRID. (section Sphagnum)andS. fallax H. KLINGGR. (section pyrosequencing using the Roche 454 GS FLX and FLX+ Titanium Cuspidata) were selected. Both bryophytes are members of the platforms performed by LGC Genomics (Berlin, Germany) and typical and cosmopolitan vegetation in peat bogs (Daniels and Eurofins MWG (Ebersberg, Germany), respectively. In total, we Eddy, 1985). Adult gametophytes of mosses were sampled in three produced 12 pyrosequencing libraries specific for Burkholderia acidic peat bogs in Austria and in three acidic peat bogs in Russia and four general bacterial pyrosequencing libraries. in September 2009 and July 2010, respectively (Table S1). Four The 16S rDNA pyrosequencing libraries were processed using single replicates per Sphagnum species (15–20 plantlets) were col- the open source software package Quantitative Insights Into lected in each of the investigated bogs at a
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