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In Planta Sporulation of Frankia spp. as a Determinant of Alder-Symbiont Interactions.
Appl Environ Microbiol. 2018 12 01; 84(23)AE

Abstract

The Alnus genus forms symbiosis with the actinobacteria Frankia spp. and ectomycorrhizal fungi. Two types of Frankia lineages can be distinguished based on their ability to sporulate in planta Spore-positive (Sp+) strains are predominant on Alnus incana and Alnus viridis in highlands, while spore-negative (Sp-) strains are mainly associated with Alnus glutinosa in lowlands. Here, we investigated whether the Sp+ predominance in nodules is due to host selection of certain Frankia genotypes from soil communities or the result of the ecological history of the alder stand soil, as well as the effect of the sporulation genotype on the ectomycorrhizal (ECM) communities. Trapping experiments were conducted using A. glutinosa, A. incana, and A. viridis plantlets on 6 soils, differing in the alder species and the frequency of Sp+ nodules in the field. Higher diversity of Frankia spp. and variation in Sp+ frequencies were observed in the trapping than in the fields. Both indigenous and trapping species shape Frankia community structure in trapped nodules. Nodulation impediments were observed under several trapping conditions in Sp+ soils, supporting a narrower host range of Sp+ Frankia species. A. incana and A. viridis were able to associate equally with compatible Sp+ and Sp- strains in the greenhouse. Additionally, no host shift was observed for Alnus-specific ECM, and the sporulation genotype of Frankia spp. defined the ECM communities on the host roots. The symbiotic association is likely determined by the host range, the soil history, and the type of in planta Frankia species. These results provide an insight into the biogeographical drivers of alder symbionts in the Holarctic region.IMPORTANCE Most Frankia-actinorhiza plant symbioses are capable of high rates of nitrogen fixation comparable to those found on legumes. Yet, our understanding of the ecology and distribution of Frankia spp. is still very limited. Several studies have focused on the distribution patterns of Frankia spp., demonstrating a combination of host and pedoclimatic parameters in their biogeography. However, very few have considered the in planta sporulation form of the strain, although it is a unique feature among all symbiotic plant-associated microbes. Compared with Sp- Frankia strains, Sp+ strains would be obligate symbionts that are highly dependent on the presence of a compatible host species and with lower efficiency in nitrogen fixation. Understanding the biogeographical drivers of Sp+ Frankia strains might help elucidate the ecological role of in planta sporulation and the extent to which this trait mediates host-partner interactions in the alder-Frankia-ECM fungal symbiosis.

Authors+Show Affiliations

Laboratoire d'Écologie Microbienne, UMR 5557, CNRS, INRA, VetAgro Sup, Université Lyon 1, Université de Lyon, Villeurbanne, France guillaume_schwob@hotmail.fr.Laboratoire Évolution et Diversité Biologique, UMR 5174, UPS, CNRS, ENFA, IRD, Université Paul Sabatier, Toulouse, France.Laboratoire d'Écologie Microbienne, UMR 5557, CNRS, INRA, VetAgro Sup, Université Lyon 1, Université de Lyon, Villeurbanne, France. Biométrie et Biologie Evolutive, UMR 5558, CNRS, INRIA, VetAgro Sup, HCL, Université Lyon 1, Université de Lyon, Villeurbanne, France.Laboratoire d'Écologie Microbienne, UMR 5557, CNRS, INRA, VetAgro Sup, Université Lyon 1, Université de Lyon, Villeurbanne, France.Laboratoire d'Écologie Microbienne, UMR 5557, CNRS, INRA, VetAgro Sup, Université Lyon 1, Université de Lyon, Villeurbanne, France.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

30217853

Citation

Schwob, G, et al. "In Planta Sporulation of Frankia Spp. as a Determinant of Alder-Symbiont Interactions." Applied and Environmental Microbiology, vol. 84, no. 23, 2018.
Schwob G, Roy M, Pozzi AC, et al. In Planta Sporulation of Frankia spp. as a Determinant of Alder-Symbiont Interactions. Appl Environ Microbiol. 2018;84(23).
Schwob, G., Roy, M., Pozzi, A. C., Herrera-Belaroussi, A., & Fernandez, M. P. (2018). In Planta Sporulation of Frankia spp. as a Determinant of Alder-Symbiont Interactions. Applied and Environmental Microbiology, 84(23). https://doi.org/10.1128/AEM.01737-18
Schwob G, et al. In Planta Sporulation of Frankia Spp. as a Determinant of Alder-Symbiont Interactions. Appl Environ Microbiol. 2018 12 1;84(23) PubMed PMID: 30217853.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - In Planta Sporulation of Frankia spp. as a Determinant of Alder-Symbiont Interactions. AU - Schwob,G, AU - Roy,M, AU - Pozzi,A C, AU - Herrera-Belaroussi,A, AU - Fernandez,M P, Y1 - 2018/11/15/ PY - 2018/07/17/received PY - 2018/09/12/accepted PY - 2018/9/16/pubmed PY - 2019/10/8/medline PY - 2018/9/16/entrez KW - Alnus KW - Frankia KW - actinorhizal symbiosis KW - ectomycorrhizae KW - host specificity KW - in planta sporulation JF - Applied and environmental microbiology JO - Appl. Environ. Microbiol. VL - 84 IS - 23 N2 - The Alnus genus forms symbiosis with the actinobacteria Frankia spp. and ectomycorrhizal fungi. Two types of Frankia lineages can be distinguished based on their ability to sporulate in planta Spore-positive (Sp+) strains are predominant on Alnus incana and Alnus viridis in highlands, while spore-negative (Sp-) strains are mainly associated with Alnus glutinosa in lowlands. Here, we investigated whether the Sp+ predominance in nodules is due to host selection of certain Frankia genotypes from soil communities or the result of the ecological history of the alder stand soil, as well as the effect of the sporulation genotype on the ectomycorrhizal (ECM) communities. Trapping experiments were conducted using A. glutinosa, A. incana, and A. viridis plantlets on 6 soils, differing in the alder species and the frequency of Sp+ nodules in the field. Higher diversity of Frankia spp. and variation in Sp+ frequencies were observed in the trapping than in the fields. Both indigenous and trapping species shape Frankia community structure in trapped nodules. Nodulation impediments were observed under several trapping conditions in Sp+ soils, supporting a narrower host range of Sp+ Frankia species. A. incana and A. viridis were able to associate equally with compatible Sp+ and Sp- strains in the greenhouse. Additionally, no host shift was observed for Alnus-specific ECM, and the sporulation genotype of Frankia spp. defined the ECM communities on the host roots. The symbiotic association is likely determined by the host range, the soil history, and the type of in planta Frankia species. These results provide an insight into the biogeographical drivers of alder symbionts in the Holarctic region.IMPORTANCE Most Frankia-actinorhiza plant symbioses are capable of high rates of nitrogen fixation comparable to those found on legumes. Yet, our understanding of the ecology and distribution of Frankia spp. is still very limited. Several studies have focused on the distribution patterns of Frankia spp., demonstrating a combination of host and pedoclimatic parameters in their biogeography. However, very few have considered the in planta sporulation form of the strain, although it is a unique feature among all symbiotic plant-associated microbes. Compared with Sp- Frankia strains, Sp+ strains would be obligate symbionts that are highly dependent on the presence of a compatible host species and with lower efficiency in nitrogen fixation. Understanding the biogeographical drivers of Sp+ Frankia strains might help elucidate the ecological role of in planta sporulation and the extent to which this trait mediates host-partner interactions in the alder-Frankia-ECM fungal symbiosis. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/30217853/In_Planta_Sporulation_of_Frankia_spp__as_a_Determinant_of_Alder_Symbiont_Interactions_ L2 - http://aem.asm.org/cgi/pmidlookup?view=long&pmid=30217853 DB - PRIME DP - Unbound Medicine ER -