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Symbiotic Diversity, Specificity and Distribution of Rhizobia In FEMS Microbiology Ecology, 91, 2015 doi: 10.1093/femsec/fiu024 Advance Access Publication Date: 8 December 2014 Research Article RESEARCH ARTICLE Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa) Benny Lemaire1,2,∗, Oscar Dlodlo1, Samson Chimphango1, Charles Stirton1, Brian Schrire3, James S. Boatwright4, Olivier Honnay2,ErikSmets2,5, Janet Sprent6,EuanK.James7 and Abraham M. Muasya1 1Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch 7701, Cape Town, South Africa, 2Plant Conservation and Population Biology, KU Leuven, Kasteelpark Arenberg 31, PO Box 2435, 3001 Heverlee, Belgium, 3Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK, 4Department of Biodiversity and Conservation Biology, University of the Western Cape, Private Bag X17, Bellville 7535, Cape Town, South Africa, 5Naturalis Biodiversity Center, Leiden University, 2300 RA Leiden, The Netherlands, 6Division of Plant Sciences, University of Dundee at JHI, Dundee DD2 5DA, UK and 7The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK ∗ Corresponding author: Plant Conservation and Population Biology, KU Leuven, Kasteelpark Arenberg 31, PO Box 02435, 3001 Heverlee, Belgium. Tel: +32-16-32-86-36; Fax: +32 16 32 19 68; E-mail: [email protected] One sentence summary: This study is the most comprehensive phylogenetic assessment of rhizobia within the Fynbos biome, showing that legumes are specifically associated with Burkholderia and Mesorhizobium, the latter underestimated within Fynbos soils. Editor: Angela Sessitsch ABSTRACT Rhizobial diversity and host preferences were assessed in 65 native Fynbos legumes of the papilionoid legume tribes Astragaleae, Crotalarieae, Genisteae, Indigofereae, Millettieae, Phaseoleae, Podalyrieae, Psoraleeae and Sesbanieae. Sequence analyses of chromosomal 16S rRNA, recA, atpD and symbiosis-related nodA, nifH genes in parallel with immunogold labelling assays identified the symbionts as alpha- (Azorhizobium, Bradyrhizobium, Ensifer, Mesorhizobium and Rhizobium) and beta-rhizobial (Burkholderia) lineages with the majority placed in the genera Mesorhizobium and Burkholderia showing a wide range of host interactions. Despite a degree of symbiotic promiscuity in the tribes Crotalarieae and Indigofereae nodulating with both alpha- and beta-rhizobia, Mesorhizobium symbionts appeared to exhibit a general host preference for the tribe Psoraleeae, whereas Burkholderia prevailed in the Podalyrieae. Although host genotype was the main factor determining rhizobial diversity, ecological factors such as soil acidity and site elevation were positively correlated with genetic variation within Mesorhizobium and Burkholderia, respectively, indicating an interplay of host and environmental factors on the distribution of Fynbos rhizobia. Key words: Burkholderia; Fynbos legumes; host preference; in situ immunogold labelling; Mesorhizobium; root nodulation Received: 6 October 2014; Accepted: 2 December 2014 C FEMS 2015. All rights reserved. For permissions, please e-mail: [email protected] 1 2 FEMS Microbiology Ecology, 2015, Vol. 91, No. 2 INTRODUCTION spp. and related genera in the tribe Mimoseae (Chen et al., 2005a, 2006, 2007, 2008; Mishra et al., 2012;Sheuet al., 2012, 2013; Bour- The Core Cape Subregion (CCR) formerly known as the Cape naud et al., 2013). Floristic Region (Manning and Goldblatt 2012) has been recog- The establishment of an effective symbiosis between nized as one of the richest areas of flowering plants in the legumes and rhizobia usually involves a complex molecular world with outstanding diversity, density and number of en- bacteria-plant dialogue based on rhizobial Nod factors and sig- demic species (Myers et al., 2000, 2003). This biodiversity hotspot, nal flavonoid-based molecules from the host plant (Masson- with a unique assemblage of vascular plants referred to as the Boivin et al., 2009). The secreted Nod factors (classified as lipochi- Fynbos (fine bush) biome, is probably the outcome of a combina- tooligosaccharides or LCOs) are mainly synthesized by common tion of stable climatic conditions promoting a persistent specia- nodulation genes that are specifically recognized by the host. tion of the Cape flora and relatively recent and rapid radiations Consequently, symbiotic nodulation genes play a crucial role in since the Miocene (Richardson et al., 2001; Linder 2005; Schnit- establishing symbiosis in rhizobial species, and have been used zler et al., 2011). Furthermore, physical heterogeneity in topog- as genetic markers to determine symbiotic diversity and host raphy and diverse soil types create a mosaic of sharply distinct specificity (Perret, Staehelin and Broughton 2000). microhabitats which also contribute to the elevated species rich- Previous rhizobial studies in the CCR have focused on only ness (Linder 2003, 2005; Cowling, Proches¸b and Partridge 2009). a few legume genera, probably housing only a fraction of the The CCR is largely semi-arid with generally nutrient-poor and total rhizobial diversity. Considering the high diversity of na- acidic soils (Witkowski and Mitchell 1987; Manning and Gold- tive legumes and the diverse low-nutrient habitats in the CCR blatt 2012). Similar to other (semi-) arid regions in the world, the which are positively linked with the belowground microbial Cape flora has a large component of Leguminosae (Fabaceae), communities (Slabbert et al., 2010), it is likely that the rhizo- with this family ranked as the second most species rich in the bial diversity is still largely unexplored. This study investigates region, following the Asteraceae (Manning and Goldblatt 2012). the rhizobia–legume interaction in the Fynbos biome, by se- The Leguminosae, with about 19 500 species and 751 gen- lecting a broad phylogenetic sample of legumes from different era (LPWG 2013), have largely colonized the land surface on soil types and biogeographical regions. We surveyed and char- Earth (excluding Antarctica), and its species are adapted to most acterized rhizobia from 14 genera in 9 tribes (Crotalarieae— terrestrial ecosystems ranging from deserts to tropical rain- Aspalathus, Crotalaria L., Rafnia Thunb.; Astragaleae—Lessertia forest, and tropical to arctic habitats (Doyle and Luckow 2003; DC.; Genisteae—Argyrolobium Eckl. and Zeyh.; Indigofereae— Lavin, Herendeen and Wojciechowski 2005;Lewiset al., 2005). In Indigofera L.; Millettieae—Tephrosia Pers.; Phaseoleae—Bolusafra the Fynbos biome, about 750 native legume species are known Kuntze; Podalyrieae—Amphithalea Eckl. and Zeyh., Podalyria to date, with the majority of these placed within the papil- Willd., Virgilia Poir.; Psoraleeae—Otholobium C.H. Stirt., Psoralea ionoid tribes Crotalarieae, Podalyrieae, Psoraleeae and Indigofer- L.; Sesbanieae—Sesbania Scop.). Three housekeeping genes (16S eae among which 634 species and 8 genera are endemic (Gold- rRNA, recA and atpD) were used to identify the symbiotic blatt and Manning 2002; Linder 2003; Manning and Goldblatt nitrogen-fixing bacteria and to elucidate their phylogenetic re- 2012). lationships. Symbiotic nodA and nifH genes were used to reveal All Leguminosae studied in the CCR nodulate with nitrogen- the evolutionary history of the symbiotic traits. The specific aims fixing soil bacteria, indicating that rhizobial symbionts are play- of this study were 2-fold: (1) to identify the rhizobial symbionts ing an important ecological role in this ecosystem (Sprent within taxonomically diverse hosts and determine nodulation 2009; Sprent and Gehlot 2010; Sprent, Odee and Dakora preferences for particular rhizobial lineages within the alpha- 2010, Sprent, Ardley and James 2013). Over the last few and beta-rhizobia; and (2) to examine the effect of ecological and decades, many rhizobial studies have surveyed and char- geographic variables on the genetic structure of rhizobial popu- acterized the rhizobia–plant interaction within diverse Cape lations. legume genera (Crotalarieae—Aspalathus L., Lebeckia Thunb.; Hypocalypteae—Hypocalyptus Thunb.; Phaseoleae—Rhynchosia Lour.; Podalyrieae—Cyclopia Vent., Podalyria Willd., Virgilia Poir.; Psoraleeae—Otholobium C.H.Stirt., Psoralea L.), describing a wide diversity of rhizobial lineages with most members placed in MATERIALS AND METHODS the genus Burkholderia (Elliott et al., 2007a; Garau et al., 2009; Legume and soil sampling Gyaneshwar et al., 2011;Beukeset al., 2013; Howieson et al., 2013), but relatively few within classical alpha-rhizobial groups Legume species were collected from 2008 to 2012 in the field (Kock 2004;Gerdinget al., 2012; Hassen et al., 2012;Kanuand from different localities, ecoregions and soil types in the CCR Dakora 2012). (Fig. 1). In total, 65 host lineages were sampled and herbarium The observed frequency and recent descriptions of new specimens of all collected plants were deposited at the Bolus Burkholderia species among many legume species investigated Herbarium, University of Cape Town for reference and detailed indicate how successfully the Fynbos biome has been colonized taxonomic identification. For each legume tribe, one represen- by these belowground mutualists (Elliott et al., 2007a;Beukes tative species is documented with photographs showing their et al., 2013;DeMeyeret al., 2013a,b, 2014; Howieson et al., 2013). native habitat (Fig. 2) and collected field nodules are illustrated The dominance of Burkholderia species in root nodules has been in Fig. 3. At every collection site, the soil acidity
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