Dataset Information

Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States).

ABSTRACT: The diversity of uncultured Frankia populations in root nodules of Alnus oblongifolia trees geographically isolated on mountaintops of central Arizona was analyzed by comparative sequence analyses of nifH gene fragments. Sequences were retrieved from Frankia populations in nodules of four trees from each of three mountaintops (n = 162) and their levels of diversity compared using spatial genetic clustering methods and single-nucleotide or 1, 3, or 5% sequence divergence thresholds. With the single-nucleotide threshold level, 45 different sequences with significant differences between the mountaintops were retrieved, with the southern site partitioning in a separate population from the two other sites. Some of these sequences were identical in nodules from different mountaintops and to those of strains isolated from around the world. A high level of diversity that resulted in the assignment of 14 clusters of sequences was also found on the 1% divergence level. Single-nucleotide and 1% divergence levels thus demonstrate microdiversity of frankiae in root nodules of A. oblongifolia trees and suggest a partitioning of diversity by site. At the 3 and 5% divergence levels, however, diversity was reduced to three clusters or one cluster, respectively, with no differentiation by mountaintop. Only at the 5% threshold level do all Frankia strains previously assigned to one genomic group cluster together.

SUBMITTER: Welsh AK

PROVIDER: S-EPMC2772444 | biostudies-literature | 2009 Nov

REPOSITORIES: biostudies-literature

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Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States).

Welsh Allana K AK Dawson Jeffrey O JO Gottfried Gerald J GJ Hahn Dittmar D

Applied and environmental microbiology 20090904 21

The diversity of uncultured Frankia populations in root nodules of Alnus oblongifolia trees geographically isolated on mountaintops of central Arizona was analyzed by comparative sequence analyses of nifH gene fragments. Sequences were retrieved from Frankia populations in nodules of four trees from each of three mountaintops (n = 162) and their levels of diversity compared using spatial genetic clustering methods and single-nucleotide or 1, 3, or 5% sequence divergence thresholds. With the sing ...[more]

PMID: 19734342

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Project description:Actinorhizal plants form nitrogen-fixing root nodules in symbiosis with soil-dwelling actinobacteria within the genus Frankia, and specific Frankia taxonomic clusters nodulate plants in corresponding host infection groups. In same-soil microcosms, we observed that some host species were nodulated (Alnus glutinosa, Alnus cordata, Shepherdia argentea, Casuarina equisetifolia) while others were not (Alnus viridis, Hippophaë rhamnoides). Nodule populations were represented by eight different sequences of nifH gene fragments. Two of these sequences characterized frankiae in S. argentea nodules, and three others characterized frankiae in A. glutinosa nodules. Frankiae in A. cordata nodules were represented by five sequences, one of which was also found in nodules from A. glutinosa and C. equisetifolia, while another was detected in nodules from A. glutinosa Quantitative PCR assays showed that vegetation generally increased the abundance of frankiae in soil, independently of the target gene (i.e., nifH or the 23S rRNA gene). Targeted Illumina sequencing of Frankia-specific nifH gene fragments detected 24 unique sequences from rhizosphere soils, 4 of which were also found in nodules, while the remaining 4 sequences in nodules were not found in soils. Seven of the 24 sequences from soils represented >90% of the reads obtained in most samples; the 2 most abundant sequences from soils were not found in root nodules, and only 2 of the sequences from soils were detected in nodules. These results demonstrate large differences between detectable Frankia populations in soil and those in root nodules, suggesting that root nodule formation is not a function of the abundance or relative diversity of specific Frankia populations in soils.IMPORTANCE The nitrogen-fixing actinobacterium Frankia forms root nodules on actinorhizal plants, with members of specific Frankia taxonomic clusters nodulating plants in corresponding host infection groups. We assessed Frankia diversity in root nodules of different host plant species, and we related specific populations to the abundance and relative distribution of indigenous frankiae in rhizosphere soils. Large differences were observed between detectable Frankia populations in soil and those in root nodules, suggesting that root nodule formation is not a function of the abundance or relative diversity of specific Frankia populations in soils but rather results from plants potentially selecting frankiae from the soil for root nodule formation. These data also highlight the necessity of using a combination of different assessment tools so as to adequately address methodological constraints that could produce contradictory data sets.

Project description: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.

Dataset Information

Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States).

Publications

Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States).

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