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Characterization of Bacteria Associated with Nodules of Two Endemic Legumes of Algeria, Hedysarum Naudinianum and H. Perrauderianum

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Characterization of Bacteria Associated with Nodules of Two Endemic Legumes of Algeria, Hedysarum Naudinianum and H. Perrauderianum Ann Microbiol (2014) 64:1065–1071 DOI 10.1007/s13213-013-0745-3 ORIGINAL ARTICLE Characterization of bacteria associated with nodules of two endemic legumes of Algeria, Hedysarum naudinianum and H. perrauderianum Asma Torche & Hayet Benhizia & Riccardo Rosselli & Ottavia Romoli & Marina Zanardo & Enrico Baldan & Sara Alberghini & Alessandra Tondello & Barbara Baldan & Amar Benguedouar & Andrea Squartini & Yacine Benhizia Received: 11 August 2013 /Accepted: 24 October 2013 /Published online: 3 December 2013 # Springer-Verlag Berlin Heidelberg and the University of Milan 2013 Abstract The root nodules of two wild legume species respiratory and cardiac infections in humans. Whereas no endemic to Algeria, Hedysarum naudinianum and He. culturable rhizobia and alike could be obtained on plates, perrauderianum, were investigated with regard to their PCR-based culture-independent approaches revealed in anatomy and histology, and the identity of the associated both plants the presence of a Mesorhizobium sp., which bacteria. Both plants were found to form root nodules in H. perrauderianum was identical to isolates nodulating with regular features and well infected by rod-shaped other legumes from Africa, European Mediterranean coun- bacteria. The culturable fraction of bacteria that could be tries, and Asia, while in H. naudinianum it bore a single obtained from surface-sterilized nodules included a prevail- nucleotide polymorphism which is so far unique for any ing presence of Enterobacteriaceae having 100 % 16S observed mesorhizobia. Data from the microsymbionts rDNA sequence identity with both Enterobacter cloacae appear to suggest interesting clues to interpret the evolu- and E. ludwigii. In H. perrauderianum,thistaxonwasthe tionary ecology of their host plants. sole cultured isolate, while from H. naudinianum we also found Bacillus, Lactobacillus, Staphylococcus, Rothia,and Keywords Hedysarum naudinianum . Hedysarum isolates that were 100 % identical to Corynebacterium perrauderianum . Mesorhizobium . Root nodules . Algeria . pseudodiphthericum, which is known to be an agent of Endophytic bacteria . Endemic legumes . SNP : : A. Torche A. Benguedouar Y. Benhizia Introduction Département de Microbiologie, Faculté des Sciences de la Nature et de la Vie, Laboratoire de Biologie Moléculaire et Cellulaire, Université Constantine 1, Route de Aïn El Bey, Constantine, Algeria Many legume plants rely on the symbiosis with nitrogen-fixing : : : : rhizobia, and an increasing number of studies is nowadays R. Rosselli O. Romoli E. Baldan A. Tondello B. Baldan addressing the bacterial associations of spontaneous legumi- Department of Biology, University of Padova, Via Ugo Bassi 58/b, nous species. Hedysarum is a genus of the Hedysareae tribe 35131 Padova, Italy featuring about 309 species distributed worldwide. The taxon : : M. Zanardo S. Alberghini A. Squartini (*) is divided in two main groups: the first includes the Alpine, Department of Agronomy Animals, Food, Natural Resources and Arctic, and Asiatic species (2n=14 chromosomes), while the ’ Environment, DAFNAE, University of Padova, Viale dell Università second harbous the Mediterranean species (2n=16) (Trifi- 16, 35020 Legnaro, Padova, Italy e-mail: [email protected] Farah and Marrakchi 2001), some of which have been repositioned in the new genus Sulla (Choi and Ohashi H. Benhizia 2003). Within the Mediterranean set of Hedysarum, our Département de Biologie Végétale, Faculté des Sciences de la Nature earlier interest has been devoted to Hedysarum coronarium, et de la Vie, Laboratoire de Génétique, Biochimie et Biotechnologies Végétales, Université Constantine 1, Route de Aïn El Bey, which exists both as a cultivated forage crop and as wild Constantine, Algeria stands. For this species, we described the new species of 1066 Ann Microbiol (2014) 64:1065–1071 host-specific nitrogen-fixing symbiont, Rhizobium sullae the three sites of Bougaa (00°00′00″N, 5°04′60″E) , Ain (Squartini et al. 2002). Subsequently, we have investigated Roua (36°19′60″N, 5°10′60″E) and Maoklane (36°23′50″N, the bacteria in Algeria within root nodules of Hedysarum 5°04′31″E), while H. perrauderianum was gathered from spinosissimum ssp. capitatum, H. pallidum and H. carnosum Ouled Tebbene (35°48′46″N, 5°06′05″E). All specimens were (Benhizia et al. 2004), whose occupants are dominated by green and healthy plants. Nodules were in non-senescent, endophytic gammaproteobacteria. Further. we covered two fully developed stage. other Mediterranean wild species of Hedysarum by studying Nodule excision was carried out as described by Vincent H. spinosissimum and H. glomeratum in Sardinia (Muresu (1970) and Beck et al. (1993). Roots were carefully cleaned et al. 2008). Subsequently. we investigated the nodule content and washed free of soil. Dry portions of roots with nodules of the relictual H. confertum (=H. humile) (Tondello et al. were stored with CaCl2 until nodule sterilization. Plants and 2011). In these studies. we showed the consistent non- their root apparati are shown in Fig. 2. culturability of the rhizobial symbionts and the occurrence of a vast array of opportunistic endophytes. Nodule microscopy Within Algeria. the genus Hedysarum includes ten species, some of which are endemic, such as H. naudinianum and Nodules were fixed in 3 % glutaraldehyde in 0.1 M cacodylate H. perrauderianum. The latter is moreover reported as buffer (pH 6.9) for 24 h at 4 °C and postfixed for 2 h at 4 °C in very localized (Abdelguerfi-Berrekia et al. 1991). These 1 % osmium tetroxide in 0.1 M cacodylate buffer, dehydrated two taxa are rather rare. H. naudinianum is found in the in a graded ethanol series, and then embedded in araldite resin. tell constantinois (mount of Bibans), in Algiers (Littoral, Thin sections (1 μm), obtained with a Reichert-Jung ultrami- Tell Atlas), in Boghar. and the north of Setif (Bougaa, Ain crotome, were stained with 1 % toluidine blue for light Roua). H. perrauderianum occurs in the region of Batna and microscopy. south of Setif (Abdelguerfi-Berrekia et al. 1988;Quezeland Santa 1962). Bacterial isolation from the nodules From ecological and conservational perspectives, the entire genus Hedysarum is regarded as a wealthy phytogenetic Root portions bearing nodules were washed free of soil under resource which is, however, increasingly endangered by running water, encaged in a fine-mesh steel holder and progressive genetic erosion due to overgrazing, irregular surface-sterilized by immersion in 95 % ethanol for 20 s, rainfall. and range land contraction, particularly in dry followed by 5 % sodium hypochlorite for 3 min, and then and semi-arid areas (Trifi-Farah et al. 2002). In such washed 7 times with sterile distilled water. Finally, nodules scenarios, it is of primary importance to determine were transferred aseptically into sterile Petri dishes and whether the rarity of given species could be due to their crushed in a drop of sterile distilled water. dependence on symbionts to ensure their nutritional The nodules suspension was plated on YMA-congo red, needs. The abundance or exiguity of the suitable inter- YMA-bromo-thymol blue, and PCA- and GPA-bromo-cresol active microorganisms deeply affects soil capability to purple (Vincent 1970). host and support plants. Both productivity and health of Tests to validate surface-sterilization of plant tissues, the crops as well as the distribution of natural vegetation including root nodules, were performed by touching are conditioned by interactions with ground microbiota, them several times on the surface of plate count agar with the most significant correlation being the presence (PCA, Difco) plates prior to isolation of the interior or absence of symbiotic or pathogenic microorganisms microbiota. The absence of colonies on these plates (Klironomos 2002). For these reasons, we deemed it was a requirement to ascertain the disinfection from important to cast light on the presence and identity of residual external bacteria. root nodule bacteria associated with the above-mentioned two CaCl2-stored dry nodules were rehydrated for 6 h in dis- endemic legume species thriving exclusively in Algeria and tilled water prior to the surface-sterilization treatment. enduring harsh conditions. DNA extraction from culturable bacteria Materials and methods Cells were lysed by resuspending a loopful of plate-grown isolated colonies in 50 μL of lysis buffer (0.25 % sodium Plant and nodule collection dodecyl sulphate, SDS 0.05 M NaOH), followed by stirring for 60 s on a vortex and heating at 95 °C for 15 min. The lysate The biological material was collected in the region of Sétif was centrifuged for 15 min at 13,400 g and 10 μLofthe (36°12′0″N, 5°24′0″E) in the East of Algeria (Fig 1); supernatant were mixed with 90 μL of sterile water. Lysates Hedysarum naudinianum whole plants were excavated in were stored at 4 °C prior to PCR. Ann Microbiol (2014) 64:1065–1071 1067 Fig. 1 Algeria showing the collection sites DNA extraction from nodules mixed with 90 μL of sterile water. Lysates were stored at 4 °C prior to PCR. For direct PCR analysis, aliquots of nodule suspensions (10 μL, irrespectively of original volume) were trans- PCR amplification of the 16S rDNA gene ferred to 50 μL of lysis buffer, [0.25 % sodium dodecyl sulphate (SDS) 0.05 M NaOH] in a 1.5-mL polypropylene One μL of the lysate containing the total DNA extracted from tube, followed by stirring for 60 s on a vortex and heating nodules was treated in a PCR BioRad I-Cycler using the two at 95 °C for 15 min. The lysate was
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