Abstract
To quantify the genetic diversity of Frankia bacteria associated with Alnus rubra in natural settings and to examine the relative importance of site age, management, and geographic location in structuring Frankia assemblages in A. rubra forests, root nodules from four A. rubra sites in the Pacific Northwest, USA were sampled. Frankia genetic diversity at each site was compared using sequence-based analyses of a 606 bp fragment of the nifH gene. At a 3% sequence similarity cutoff, a total of 5 Frankia genotypes were identified from 317 successfully sequenced nodules. Sites varied in the total number of genotypes present, but were typically dominated by only one or two genotypes. Phylogenetic analyses showed that all of the A. rubra-Frankia genotypes grouped with other Alnus-infective Frankia. Analysis of similarity (ANOSIM) and chi-square analyses indicated that Frankia assemblages were more strongly influenced by site age/management than geographic location. This study demonstrates that the Frankia assemblages in A. rubra forests have low genotype diversity, but that genotype abundance can differ significantly in forests of different age/management history.
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Acknowledgments
The authors thank D. Hibbs for help with use of the study sites, D. Hahn for advice about Frankia molecular protocols; D. Myrold and D. Benson for discussions about Frankia biology; A. Lundgren, A. Lipus, E. Oppelt, and J. Schouboe for lab assistance; A. Lipus and two anonymous reviewers for constructive comments on a previous version of this manuscript. Funding was provided by the M.J. Murdock Charitable Trust, Lewis & Clark College, and the National Science Foundation (DEB-0742696).
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Figure S1
Phylogenetic reconstruction of 17 Frankia taxa based on 522 bp of the nifH gene. This analysis was conducted to determine to which host infection group the A. rubra genotypes encountered in this study belonged. A representative of the five Alnus-infective (A1–A5) and four Elaeagnus-infective (E1–E4) sub-groups of Welsh et al. (2009a), a single representative of each A. rubra KL genotype, and the genome sequences of strains ACN14a and Ean1pec were included. Nodes are labeled with posterior probabilities from Bayesian analysis and, in parentheses, aLRT scores from Maximum Likelihood (ML) analysis. Dashes indicates that branch was not present in the Bayesian analysis. Taxa are labeled with GenBank accession number in parentheses. A Frankia sequence from Datisca cannabina was designated as the outgroup following Welsh et al. (2009a). (PS 279 kb)
Appendices
Appendix 1
Molecular analyses of Frankia nodules and experimental tests of sampling methodology
Amplification and sequencing of Frankia nifH
Within 48 h of field collection, individual nodules were surface sterilized by manual agitation in a 10% bleach solution for 2 min. The nodules were then rinsed three times with deionized water and stored at −20°C prior to DNA extraction. To extract total genomic DNA, 1–2 lobes from single individual nodule samples were macerated in 180 µL of buffer ATL from the Qiagen DNA Tissue 200 Kit (Qiagen, Carlsbad, CA). The periderm of each nodule sample was not removed prior to maceration (see below for justification). One hundred eighty µL of 20 mg/mL lysozyme was added to the homogenized tissue solution and incubated at 37°C for 30 min, as recommended for Gram-positive bacteria. The remainder of the DNA extraction was performed according to the manufacturer’s instructions.
The polymerase chain reaction (PCR) was used to amplify a 606 bp fragment of the nifH gene with the Frankia-specific primer pair nifHf1 (5′-GGC AAG TCC ACC ACC CAG C-3′) and nifHr (5′-CTC GAT GAC CGT CAT CCG GC-3′). This region was chosen because it has previously been demonstrated to differentiate among closely related Frankia genotypes occurring on the same host plant species (Welsh et al 2009a; Mirza et al. 2009; Kennedy et al. 2010). PCR amplifications were performed in 20 µL reactions containing: 0.5 µL bulk DNA, 0.4 µL of each primer (10 µM), 10 µL MasterAmp F PCR buffer (Epicenter, Madison, WI) and 0.75 U Taq Polymerase (New England Biolabs, Ipswich, MA). Samples that did not successfully amplify initially were re-run using 1:20 dilutions of the DNA template. PCR cycling conditions were as follows: 96°C for 5 min; 35 cycles at 96°C for 30 s, 64°C for 30 s, and 72°C for 45 s; and a final 7 min 72°C extension. Amplification was checked with electrophoresis on 1.5% agarose gels (GenePure LE, ISC BioExpress, Kaysville, UT). Gels were stained with ethidium bromide and visualized under UV fluorescence. All successful PCR products were cleaned using 1.5 uL of ExoSAP IT (USB Corp., Cleveland, OH) with 7.5 uL of DNA and incubated at 37°C for 45 min, followed by 80°C for 15 min. Sequencing was performed on a 3730xl DNA Analyzer (Applied Biosystems, Foster City, CA) at the Genomic Analysis and Technology Core Facility at the University of Arizona, USA.
Experimental tests of sampling methodology
To ensure our results were not biased by sampling methodology, two other analyses were performed. Previous Frankia studies on other hosts have found multiple strains per nodule (Reddell and Bowen 1985), so we tested whether multiple samples (i.e. different lobes) from the same nodule belonged to the same genotype. Five nodules were collected from multiple A. rubra individuals at Tryon Creek State Park in Portland, Oregon (N 45′27.139″, W 122′40.153″). Four lobes per nodule were removed and independently identified using the same methods described above. In all cases, the same genotype was recovered from the individual lobes of each nodule, indicating our nodule sampling method accurately captured Frankia genotype nodule richness. We also compared the interior versus periderm tissues of nine nodules from the same location to determine if periderm removal influenced genotype richness. In eight of the nine nodules, the genotype composition was identical between tissues. For the one nodule with non-matching genotypes, we believe this result was most likely caused by incomplete surface sterilization. Both of these analyses make us confident that the nodule sampling methodology did not significantly influence the observed patterns of genotype diversity.
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Appendix 2
Site information for samples from which a clear nifH sequence was obtained. Samples sharing the same GenBank accession number were identical across the 518 base pairs analyzed. Site abbreviations are as follows: FC = Fox Creek, M = Mt. Hood, T = Toledo, TC = Thompson Cat.
Genotype | Site | Sample | GenBank Accession # |
|---|---|---|---|
KL1 | FC | 3 | GU810473 |
KL1 | FC | 26 | GU810473 |
KL1 | FC | 28 | GU810473 |
KL1 | FC | 32 | GU810473 |
KL1 | FC | 42 | GU810473 |
KL1 | FC | 49 | GU810473 |
KL1 | FC | 55 | GU810473 |
KL1 | FC | 62 | GU810473 |
KL1 | FC | 66 | GU810473 |
KL1 | FC | 67 | GU810473 |
KL1 | FC | 68 | GU810473 |
KL1 | FC | 76 | GU810473 |
KL1 | FC | 77 | GU810473 |
KL1 | FC | 78 | GU810473 |
KL1 | FC | 81 | GU810473 |
KL1 | FC | 82 | GU810473 |
KL1 | FC | 89 | GU810473 |
KL1 | FC | 92 | GU810473 |
KL1 | FC | 94 | GU810473 |
KL1 | FC | 95 | GU810473 |
KL1 | FC | 96 | GU810473 |
KL1 | FC | 98 | GU810473 |
KL1 | FC | 99 | GU810473 |
KL1 | FC | 100 | GU810473 |
KL1 | FC | 101 | GU810473 |
KL1 | T | 1 | GU810473 |
KL1 | T | 2 | GU810473 |
KL1 | T | 3 | GU810473 |
KL1 | T | 5 | GU810473 |
KL1 | T | 6 | GU810473 |
KL1 | T | 7 | GU810473 |
KL1 | T | 8 | GU810473 |
KL1 | T | 9 | GU810473 |
KL1 | T | 10 | GU810473 |
KL1 | T | 11 | GU810473 |
KL1 | T | 12 | GU810473 |
KL1 | T | 13 | GU810473 |
KL1 | T | 14 | GU810473 |
KL1 | T | 15 | GU810473 |
KL1 | T | 16 | GU810473 |
KL1 | T | 17 | GU810473 |
KL1 | T | 18 | GU810473 |
KL1 | T | 19 | GU810473 |
KL1 | T | 20 | GU810473 |
KL1 | T | 21 | GU810473 |
KL1 | T | 22 | GU810473 |
KL1 | T | 23 | GU810473 |
KL1 | T | 24 | GU810473 |
KL1 | T | 25 | GU810473 |
KL1 | T | 29 | GU810473 |
KL1 | T | 30 | GU810473 |
KL1 | T | 31 | GU810473 |
KL1 | T | 32 | GU810473 |
KL1 | T | 33 | GU810473 |
KL1 | T | 34 | GU810473 |
KL1 | T | 36 | GU810473 |
KL1 | T | 38 | GU810473 |
KL1 | T | 39 | GU810473 |
KL1 | T | 40 | GU810473 |
KL1 | T | 41 | GU810473 |
KL1 | T | 44 | GU810473 |
KL1 | T | 45 | GU810473 |
KL1 | T | 46 | GU810473 |
KL1 | T | 48 | GU810473 |
KL1 | T | 49 | GU810473 |
KL1 | T | 51 | GU810473 |
KL1 | T | 52 | GU810473 |
KL1 | T | 53 | GU810473 |
KL1 | T | 54 | GU810473 |
KL1 | T | 55 | GU810473 |
KL1 | T | 56 | GU810473 |
KL1 | T | 57 | GU810473 |
KL1 | T | 59 | GU810473 |
KL1 | T | 60 | GU810473 |
KL1 | T | 61 | GU810473 |
KL1 | T | 62 | GU810473 |
KL1 | T | 63 | GU810473 |
KL1 | T | 64 | GU810473 |
KL1 | T | 65 | GU810473 |
KL1 | T | 66 | GU810473 |
KL1 | T | 67 | GU810473 |
KL1 | T | 68 | GU810473 |
KL1 | T | 69 | GU810473 |
KL1 | T | 70 | GU810473 |
KL1 | T | 71 | GU810473 |
KL1 | T | 72 | GU810473 |
KL1 | T | 73 | GU810473 |
KL1 | T | 75 | GU810473 |
KL1 | T | 77 | GU810473 |
KL1 | T | 78 | GU810473 |
KL1 | T | 79 | GU810473 |
KL1 | T | 80 | GU810473 |
KL1 | T | 81 | GU810473 |
KL1 | T | 82 | GU810473 |
KL1 | T | 83 | GU810473 |
KL1 | T | 84 | GU810473 |
KL1 | T | 85 | GU810473 |
KL1 | T | 87 | GU810473 |
KL1 | T | 88 | GU810473 |
KL1 | T | 89 | GU810473 |
KL1 | T | 90 | GU810473 |
KL1 | T | 91 | GU810473 |
KL1 | T | 92 | GU810473 |
KL1 | T | 93 | GU810473 |
KL1 | T | 96 | GU810473 |
KL1 | T | 97 | GU810473 |
KL1 | T | 98 | GU810473 |
KL1 | T | 99 | GU810473 |
KL1 | TC | 3 | GU810473 |
KL1 | TC | 10 | GU810473 |
KL1 | TC | 18 | GU810473 |
KL1 | TC | 52 | GU810473 |
KL1 | TC | 100 | GU810473 |
KL1.1 | M | 71 | HM031938 |
KL1.2 | TC | 100 | HM031939 |
KL1.2 | TC | 95 | HM031939 |
KL1.2 | TC | 91 | HM031939 |
KL1.2 | TC | 85 | HM031939 |
KL1.2 | TC | 76 | HM031939 |
KL1.2 | TC | 67 | HM031939 |
KL1.2 | TC | 60 | HM031939 |
KL1.2 | TC | 54 | HM031939 |
KL1.2 | TC | 5 | HM031939 |
KL1.2 | M | 92 | HM031939 |
KL1.2 | M | 84 | HM031939 |
KL1.2 | M | 81 | HM031939 |
KL1.2 | M | 73 | HM031939 |
KL1.2 | M | 52 | HM031939 |
KL1.2 | M | 14 | HM031939 |
KL1.2 | TC | 28 | HM031939 |
KL1.2 | TC | 61 | HM031939 |
KL1.2 | TC | 59 | HM031939 |
KL1.3 | TC | 84 | HM031940 |
KL1.3 | TC | 83 | HM031940 |
KL1.3 | TC | 79 | HM031940 |
KL1.3 | TC | 77 | HM031940 |
KL1.3 | TC | 71 | HM031940 |
KL1.3 | TC | 68 | HM031940 |
KL1.3 | TC | 66 | HM031940 |
KL1.3 | TC | 64 | HM031940 |
KL1.3 | M | 64 | HM031940 |
KL1.4 | M | 99 | HM031941 |
KL1.4 | M | 44 | HM031941 |
KL1.4 | M | 43 | HM031941 |
KL1.4 | M | 42 | HM031941 |
KL1.4 | M | 41 | HM031941 |
KL1.4 | M | 40 | HM031941 |
KL1.4 | M | 30 | HM031941 |
KL1.4 | M | 29 | HM031941 |
KL1.4 | M | 27 | HM031941 |
KL1.4 | M | 2 | HM031941 |
KL1.5 | FC | 87 | HM031942 |
KL1.5 | TC | 90 | HM031942 |
KL1.5 | TC | 82 | HM031942 |
KL1.5 | TC | 70 | HM031942 |
KL1.5 | TC | 6 | HM031942 |
KL1.5 | TC | 17 | HM031942 |
KL1.5 | TC | 19 | HM031942 |
KL1.5 | TC | 26 | HM031942 |
KL1.5 | TC | 31 | HM031942 |
KL1.5 | TC | 33 | HM031942 |
KL1.5 | TC | 37 | HM031942 |
KL1.5 | TC | 40 | HM031942 |
KL1.5 | TC | 57 | HM031942 |
KL1.5 | TC | 65 | HM031942 |
KL1.5 | TC | 74 | HM031942 |
KL1.5 | TC | 81 | HM031942 |
KL1.5 | TC | 78 | HM031942 |
KL1.6 | M | 50 | HM031943 |
KL1.7 | TC | 39 | HM031944 |
KL1.7 | M | 93 | HM031944 |
KL1.7 | M | 87 | HM031944 |
KL1.8 | M | 96 | HM031945 |
KL1.9 | M | 89 | HM031946 |
KL1.10 | M | 83 | HM031947 |
KL1.10 | M | 51 | HM031947 |
KL1.10 | M | 36 | HM031947 |
KL1.11 | M | 85 | HM031948 |
KL1.11 | M | 82 | HM031948 |
KL1.11 | M | 79 | HM031948 |
KL1.11 | M | 69 | HM031948 |
KL1.11 | M | 62 | HM031948 |
KL1.12 | TC | 20 | HM031949 |
KL1.13 | TC | 13 | HM031950 |
KL1.14 | TC | 53 | HM031951 |
KL1.14 | TC | 51 | HM031951 |
KL1.14 | TC | 50 | HM031951 |
KL2 | FC | 1 | GU810474 |
KL2 | FC | 5 | GU810474 |
KL2 | FC | 8 | GU810474 |
KL2 | FC | 10 | GU810474 |
KL2 | FC | 11 | GU810474 |
KL2 | FC | 12 | GU810474 |
KL2 | FC | 13 | GU810474 |
KL2 | FC | 18 | GU810474 |
KL2 | FC | 19 | GU810474 |
KL2 | FC | 20 | GU810474 |
KL2 | FC | 21 | GU810474 |
KL2 | FC | 22 | GU810474 |
KL2 | FC | 23 | GU810474 |
KL2 | FC | 24 | GU810474 |
KL2 | FC | 27 | GU810474 |
KL2 | FC | 29 | GU810474 |
KL2 | FC | 31 | GU810474 |
KL2 | FC | 33 | GU810474 |
KL2 | FC | 34 | GU810474 |
KL2 | FC | 35 | GU810474 |
KL2 | FC | 37 | GU810474 |
KL2 | FC | 38 | GU810474 |
KL2 | FC | 39 | GU810474 |
KL2 | FC | 40 | GU810474 |
KL2 | FC | 41 | GU810474 |
KL2 | FC | 45 | GU810474 |
KL2 | FC | 46 | GU810474 |
KL2 | FC | 47 | GU810474 |
KL2 | FC | 51 | GU810474 |
KL2 | FC | 59 | GU810474 |
KL2 | FC | 61 | GU810474 |
KL2 | FC | 63 | GU810474 |
KL2 | FC | 65 | GU810474 |
KL2 | FC | 71 | GU810474 |
KL2 | FC | 72 | GU810474 |
KL2 | M | 1 | GU810474 |
KL2 | M | 3 | GU810474 |
KL2 | M | 4 | GU810474 |
KL2 | M | 5 | GU810474 |
KL2 | M | 6 | GU810474 |
KL2 | M | 7 | GU810474 |
KL2 | M | 8 | GU810474 |
KL2 | M | 9 | GU810474 |
KL2 | M | 10 | GU810474 |
KL2 | M | 11 | GU810474 |
KL2 | M | 12 | GU810474 |
KL2 | M | 15 | GU810474 |
KL2 | M | 16 | GU810474 |
KL2 | M | 17 | GU810474 |
KL2 | M | 18 | GU810474 |
KL2 | M | 19 | GU810474 |
KL2 | M | 20 | GU810474 |
KL2 | M | 23 | GU810474 |
KL2 | M | 25 | GU810474 |
KL2 | M | 28 | GU810474 |
KL2 | M | 31 | GU810474 |
KL2 | M | 33 | GU810474 |
KL2 | M | 37 | GU810474 |
KL2 | M | 45 | GU810474 |
KL2 | M | 46 | GU810474 |
KL2 | M | 47 | GU810474 |
KL2 | M | 48 | GU810474 |
KL2 | M | 49 | GU810474 |
KL2 | M | 53 | GU810474 |
KL2 | M | 55 | GU810474 |
KL2 | M | 59 | GU810474 |
KL2 | M | 60 | GU810474 |
KL2 | M | 61 | GU810474 |
KL2 | M | 63 | GU810474 |
KL2 | M | 66 | GU810474 |
KL2 | M | 67 | GU810474 |
KL2 | M | 68 | GU810474 |
KL2 | M | 72 | GU810474 |
KL2 | M | 75 | GU810474 |
KL2 | M | 76 | GU810474 |
KL2 | M | 78 | GU810474 |
KL2 | M | 80 | GU810474 |
KL2 | M | 86 | GU810474 |
KL2 | M | 88 | GU810474 |
KL2 | M | 90 | GU810474 |
KL2 | M | 91 | GU810474 |
KL2 | M | 94 | GU810474 |
KL2 | M | 97 | GU810474 |
KL2 | M | 98 | GU810474 |
KL2 | M | 100 | GU810474 |
KL2 | T | 86 | GU810474 |
KL2 | T | 42 | GU810474 |
KL2 | TC | 43 | GU810474 |
KL2 | TC | 21 | GU810474 |
KL2 | TC | 23 | GU810474 |
KL2 | TC | 24 | GU810474 |
KL2 | TC | 75 | GU810474 |
KL2.1 | TC | 7 | HM031952 |
KL2.2 | M | 56 | HM031953 |
KL2.2 | M | 54 | HM031953 |
KL2.2 | M | 26 | HM031953 |
KL2.3 | TC | 99 | HM031954 |
KL2.3 | M | 39 | HM031954 |
KL2.3 | M | 34 | HM031954 |
KL2.3 | M | 21 | HM031954 |
KL2.4 | TC | 22 | HM031955 |
KL2.4 | FC | 30 | HM031955 |
KL2.4 | FC | 43 | HM031955 |
KL2.4 | FC | 48 | HM031955 |
KL2.5 | FC | 6 | HM031956 |
KL2.5 | FC | 9 | HM031956 |
KL2.5 | FC | 15 | HM031956 |
KL2.5 | M | 22 | HM031956 |
KL2.5 | TC | 16 | HM031956 |
KL2.6 | FC | 14 | HM031957 |
KL3 | T | 4 | GU810475 |
KL3 | TC | 8 | GU810475 |
KL3 | TC | 38 | GU810475 |
KL3 | TC | 41 | GU810475 |
KL3 | TC | 42 | GU810475 |
KL3.1 | TC | 12 | HM031958 |
KL3.1 | T | 50 | HM031958 |
KL3.2 | TC | 46 | HM031959 |
KL4 | TC | 98 | GU810476 |
KL4 | T | 76 | GU810476 |
KL4 | FC | 52 | GU810476 |
KL5 | M | 24 | GU810477 |
KL5.1 | TC | 36 | HM031959 |
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Kennedy, P.G., Weber, M.G. & Bluhm, A.A. Frankia bacteria in Alnus rubra forests: genetic diversity and determinants of assemblage structure. Plant Soil 335, 479–492 (2010). https://doi.org/10.1007/s11104-010-0436-9
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DOI: https://doi.org/10.1007/s11104-010-0436-9