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, 6 (8), e23742

Global Distribution of Polaromonas Phylotypes--Evidence for a Highly Successful Dispersal Capacity

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Global Distribution of Polaromonas Phylotypes--Evidence for a Highly Successful Dispersal Capacity

John L Darcy et al. PLoS One.

Abstract

Bacteria from the genus Polaromonas are dominant phylotypes in clone libraries and culture collections from polar and high-elevation environments. Although Polaromonas has been found on six continents, we do not know if the same phylotypes exist in all locations or if they exhibit genetic isolation by distance patterns. To examine their biogeographic distribution, we analyzed all available, long-read 16S rRNA gene sequences of Polaromonas phylotypes from glacial and periglacial environments across the globe. Using genetic isolation by geographic distance analyses, including Mantel tests and Mantel correlograms, we found that Polaromonas phylotypes are globally distributed showing weak isolation by distance patterns at global scales. More focused analyses using discrete, equally sampled distances classes, revealed that only two distance classes (out of 12 total) showed significant spatial structuring. Overall, our analyses show that most Polaromonas phylotypes are truly globally distributed, but that some, as yet unknown, environmental variable may be selecting for unique phylotypes at a minority of our global sites. Analyses of aerobiological and genomic data suggest that Polaromonas phylotypes are globally distributed as dormant cells through high-elevation air currents; Polaromonas phylotypes are common in air and snow samples from high altitudes, and a glacial-ice metagenome and the two sequenced Polaromonas genomes contain the gene hipA, suggesting that Polaromonas can form dormant cells.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Locations of worldwide sampling sites on 6 continents.
Antarctic locations are inset, with Prime Meridian noted. Alphabetic labels (A – L) for location markers correspond to the those of Table 1 and Table S1.
Figure 2
Figure 2. Maximum-likelihood phylogenetic tree showing the diversity, geographic distribution and sub-clade groupings of the Polaromonas monophyletic clade.
Tree is rooted with sequences of Rhodoferrax and Variovorax. Nodes with annotations are well supported by both Baysian and maximum-likelihood trees (posterior probability values above 60%, bootstrap support above 60%, respectively). Sequence names or accession numbers are color-coded by geographic regions. Guide sequences of well-described Polaromonas species and strains are shown to confirm that the clade depicted is equivalent to the genus Polaromonas.
Figure 3
Figure 3. All pairwise comparisons of genetic distance by geographic distance for glacier-associated Polaromonas sequences (n = 1378).
There was a slight (r M = 0.09) but significant (P = 0.01, Mantel test) increase in genetic distance with geographic distance for the entire data set, but a Mantel correlogram (Figure 4) revealed that spatial structuring was not evident in 10 out of 12 total distance classes across the globe. This pattern was maintained even when only the hyper-variable regions of the 16S rRNA gene were analyzed (see Figure S1). The largest geographic distance comparison in this study was 18,838 km, between the Collins Glacier in Antarctica and the John Evans glacier in Nunavut, Canada. Circle size is proportional to the number of pair wise comparisons at each point on the plot, with bin sizes of 1, 2, 3–4, 5, and >5 for the smallest to largest circles.
Figure 4
Figure 4. Mantel Correlogram showing spatial structuring of Polaromonas phylotypes within different distance classes (the midpoint of each distance class is plotted).
Shaded diamonds represent distance classes which contained statistically significant spatial structuring as determined using Mantel test on each distance class, and comparing the test's P-value after applying the Bonferroni correction (corrected alpha = 0.004). Unlike previous studies that used this approach to show spatial structuring at large scales , our data clearly show that a minority of distance classes indicate significant isolation by distance patterns supporting our contention that Polaromonas phylotypes are globally distributed.

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