Adaptation and Incipient Sympatric Speciation of Bacillus Simplex Under Microclimatic Contrast at "Evolution Canyons" I and II, Israel

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2005 Oct 27

PMID 16249328

Citations 41

Authors

Johannes Sikorski

Eviatar Nevo

Affiliations

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Abstract

The microevolutionary dynamics of prokaryotes in natural habitats, such as soil, is poorly understood in contrast to our increasing knowledge on their immense diversity. We performed microevolutionary analyses on 945 soil isolates of Bacillus simplex from "Evolution Canyons" I (Carmel, Israel) and II (Galilee, Israel). These canyons represent similar ecological replicates, separated by 40 km, with highly contrasting interslope abiotic and biotic conditions in each (within a distance of only 100-400 m). Strains representing genetic groups were identical in their 16S sequences, suggesting high genetic similarity and monophyletic origin. Parallel and nested phylogenetic structures correlated with ecological contrasts rather than geographical distance. Additionally, slope-specific populations differed substantially in their diversity. The levels of DNA repair (determined by UV sensitivity) and spontaneous mutation rate (resistance to rifampicin) relate to ecological stress and phylogeny. Altogether, the results suggest adaptive radiation at a microscale. We discuss the observed adaptive population structures in the context of incipient sympatric speciation in soil bacteria. We conclude that, despite different biology, prokaryotes, like sexually reproducing eukaryotes, may consist of true species and parallel ecological speciation in eukaryotes.

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References

Heyrman J, Logan N, Rodriguez-Diaz M, Scheldeman P, Lebbe L, Swings J . Study of mural painting isolates, leading to the transfer of 'Bacillus maroccanus' and 'Bacillus carotarum' to Bacillus simplex, emended description of Bacillus simplex, re-examination of the strains previously attributed to 'Bacillus macroides' and.... Int J Syst Evol Microbiol. 2005; 55(Pt 1):119-131. DOI: 10.1099/ijs.0.63221-0. View

Sniegowski P, Gerrish P, Johnson T, Shaver A . The evolution of mutation rates: separating causes from consequences. Bioessays. 2000; 22(12):1057-66. DOI: 10.1002/1521-1878(200012)22:12<1057::AID-BIES3>3.0.CO;2-W. View

Duncan K, Ferguson N, Kimura K, Zhou X, Istock C . FINE-SCALE GENETIC AND PHENOTYPIC STRUCTURE IN NATURAL POPULATIONS OF BACILLUS SUBTILIS AND BACILLUS LICHENIFORMIS: IMPLICATIONS FOR BACTERIAL EVOLUTION AND SPECIATION. Evolution. 2017; 48(6):2002-2025. DOI: 10.1111/j.1558-5646.1994.tb02229.x. View

Kassen R, Llewellyn M, Rainey P . Ecological constraints on diversification in a model adaptive radiation. Nature. 2004; 431(7011):984-8. DOI: 10.1038/nature02923. View

Lawrence J . Gene transfer in bacteria: speciation without species?. Theor Popul Biol. 2002; 61(4):449-60. DOI: 10.1006/tpbi.2002.1587. View

Townsend J, Nielsen K, Fisher D, Hartl D . Horizontal acquisition of divergent chromosomal DNA in bacteria: effects of mutator phenotypes. Genetics. 2003; 164(1):13-21. PMC: 1462543. DOI: 10.1093/genetics/164.1.13. View

Nevo E . Evolution in action across phylogeny caused by microclimatic stresses at "Evolution Canyon". Theor Popul Biol. 1998; 52(3):231-43. DOI: 10.1006/tpbi.1997.1330. View

Gevers D, Cohan F, Lawrence J, Spratt B, Coenye T, Feil E . Opinion: Re-evaluating prokaryotic species. Nat Rev Microbiol. 2005; 3(9):733-9. DOI: 10.1038/nrmicro1236. View

Tanaka M, Bergstrom C, Levin B . The evolution of mutator genes in bacterial populations: the roles of environmental change and timing. Genetics. 2003; 164(3):843-54. PMC: 1462624. DOI: 10.1093/genetics/164.3.843. View

10.

Welsh J, McClelland M . Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res. 1990; 18(24):7213-8. PMC: 332855. DOI: 10.1093/nar/18.24.7213. View

11.

Sikorski J, Rossello-Mora R, Lorenz M . Analysis of genotypic diversity and relationships among Pseudomonas stutzeri strains by PCR-based genomic fingerprinting and multilocus enzyme electrophoresis. Syst Appl Microbiol. 1999; 22(3):393-402. DOI: 10.1016/S0723-2020(99)80048-4. View

12.

Nevo E . Evolution of genome-phenome diversity under environmental stress. Proc Natl Acad Sci U S A. 2001; 98(11):6233-40. PMC: 33451. DOI: 10.1073/pnas.101109298. View

13.

Lupu A, Pechkovskaya A, Rashkovetsky E, Nevo E, Korol A . DNA repair efficiency and thermotolerance in Drosophila melanogaster from "Evolution Canyon". Mutagenesis. 2004; 19(5):383-90. DOI: 10.1093/mutage/geh045. View

14.

Oda Y, Wanders W, Huisman L, Meijer W, Gottschal J, Forney L . Genotypic and phenotypic diversity within species of purple nonsulfur bacteria isolated from aquatic sediments. Appl Environ Microbiol. 2002; 68(7):3467-77. PMC: 126784. DOI: 10.1128/AEM.68.7.3467-3477.2002. View

15.

McArthur J, Kovacic D, Smith M . Genetic diversity in natural populations of a soil bacterium across a landscape gradient. Proc Natl Acad Sci U S A. 1988; 85(24):9621-4. PMC: 282817. DOI: 10.1073/pnas.85.24.9621. View

16.

Jolley K, Feil E, Chan M, Maiden M . Sequence type analysis and recombinational tests (START). Bioinformatics. 2001; 17(12):1230-1. DOI: 10.1093/bioinformatics/17.12.1230. View

17.

Papke R, Koenig J, Rodriguez-Valera F, Doolittle W . Frequent recombination in a saltern population of Halorubrum. Science. 2004; 306(5703):1928-9. DOI: 10.1126/science.1103289. View

18.

Rossello-Mora R, Amann R . The species concept for prokaryotes. FEMS Microbiol Rev. 2001; 25(1):39-67. DOI: 10.1111/j.1574-6976.2001.tb00571.x. View

19.

Saleem M, Lamb B, Nevo E . Inherited differences in crossing over and gene conversion frequencies between wild strains of Sordaria fimicola from "Evolution Canyon". Genetics. 2002; 159(4):1573-93. PMC: 1461899. DOI: 10.1093/genetics/159.4.1573. View

20.

Sikorski J, Mohle M, Wackernagel W . Identification of complex composition, strong strain diversity and directional selection in local Pseudomonas stutzeri populations from marine sediment and soils. Environ Microbiol. 2002; 4(8):465-76. DOI: 10.1046/j.1462-2920.2002.00325.x. View