BACKGROUND: Distribution and evolutionary history of resistance genes in environmental actinobacteria provide information on intensity of antibiosis and evolution of specific secondary metabolic pathways at a given site. To this day, actinobacteria producing biologically active compounds were isolated mostly from soil but only a limited range of soil environments were commonly sampled. Consequently, soil remains an unexplored environment in search for novel producers and related evolutionary questions. RESULTS: Ninety actinobacteria strains isolated at contrasting soil sites were characterized phylogenetically by 16S rRNA gene, for presence of erm and ABC transporter resistance genes and antibiotic production. An analogous analysis was performed in silico with 246 and 31 strains from Integrated Microbial Genomes (JGI_IMG) database selected by the presence of ABC transporter genes and erm genes, respectively. In the isolates, distances of erm gene sequences were significantly correlated to phylogenetic distances based on 16S rRNA genes, while ABC transporter gene distances were not. The phylogenetic distance of isolates was significantly correlated to soil pH and organic matter content of isolation sites. In the analysis of JGI_IMG datasets the correlation between phylogeny of resistance genes and the strain phylogeny based on 16S rRNA genes or five housekeeping genes was observed for both the erm genes and ABC transporter genes in both actinobacteria and streptomycetes. However, in the analysis of sequences from genomes where both resistance genes occurred together the correlation was observed for both ABC transporter and erm genes in actinobacteria but in streptomycetes only in the erm gene. CONCLUSIONS: The type of erm resistance gene sequences was influenced by linkage to 16S rRNA gene sequences and site characteristics. The phylogeny of ABC transporter gene was correlated to 16S rRNA genes mainly above the genus level. The results support the concept of new specific secondary metabolite scaffolds occurring more likely in taxonomically distant producers but suggest that the antibiotic selection of gene pools is also influenced by site conditions.

Analytical and Testing Laboratory Research Institute of Brewing and Malting PLC Prague Czech Republic

Department of Probability and Mathematical Statistics Faculty of Mathematics and Physics Charles University Prague Czech Republic

Epidemiology and Ecology of Microorganisms Crop Research Institute Prague Czech Republic

Faculty of Pharmacy Charles University Hradec Kralove Czech Republic

Laboratory for Biology of Secondary Metabolism Institute of Microbiology of the AS CR v v i Prague Czech Republic

Laboratory of Fungal Genetics and Metabolism Institute of Microbiology of the AS CR v v i Prague Czech Republic

Oceanography Section Science Research Center Kochi University IMT MEXT Kochi Japan

See more in PubMed

Jousset A, Eisenhauer N, Materne E, Scheu S. Evolutionary history predicts the stability of cooperation in microbial communities. Nature Comm. 2013;4:2573. doi: 10.1038/ncomms3573. PubMed DOI

Ziemert N, Lechner A, Wietz M, Millán-Aguiñaga N, Chavarria KL, Jensen PR. Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora. Proc Natl Acad Sci U S A. 2014;111:E1130–E1139. doi: 10.1073/pnas.1324161111. PubMed DOI PMC

Reddy BV, Kallifidas D, Kim JH, Charlop Powers Z, Feng Z, Brady SF. Natural product biosynthetic gene diversity in geographically distinct soil microbiomes. Appl Environ Microbiol. 2012;78:3744–3752. doi: 10.1128/AEM.00102-12. PubMed DOI PMC

Laskaris P, Tolba S, Calvo-Bado L, Wellington L. Coevolution of antibiotic production and counter-resistance in soil bacteria. Environ Microbiol. 2010;12:783–796. doi: 10.1111/j.1462-2920.2009.02125.x. PubMed DOI

Hohmann C, Schneider K, Bruntner C, Irran E, Nicholson G, Bull AT, et al. Caboxamycin, a new antibiotic of the benzoxazole family produced by the deep-sea strain Streptomyces sp. NTK 937. J Antibiot. 2009;62:99–104. doi: 10.1038/ja.2008.24. PubMed DOI

Genilloud O, Gonzalez I, Salazar O, Martin J, Tormo JR, Vicente F. Current approaches to exploit actinomycetes as a source of novel natural products. J Ind Microbiol Biotechnol. 2011;38:375–389. doi: 10.1007/s10295-010-0882-7. PubMed DOI

Polz MF, Alm EJ, Hanage WP. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 2013;29:170–175. doi: 10.1016/j.tig.2012.12.006. PubMed DOI PMC

Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010;74:417–433. doi: 10.1128/MMBR.00016-10. PubMed DOI PMC

Thaker MN, Wang W, Spanogiannopoulos P, Waglechner N, King AM, Medina R, et al. Identifying producers of antibacterial compounds by screening for antibiotic resistance. Nat Biotechnol. 2013;31:922–927. doi: 10.1038/nbt.2685. PubMed DOI

Chopra I, Hesse L, O'Neill AJ. Exploiting current understanding of antibiotic action for discovery of new drugs. J Appl Microbiol. 2002;92:4S–15S. doi: 10.1046/j.1365-2672.92.5s1.13.x. PubMed DOI

Aminov RI, Mackie RI. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol Lett. 2007;271:147–161. doi: 10.1111/j.1574-6968.2007.00757.x. PubMed DOI

Peschke U, Schmidt H, Zhang H-Z, Piepersberg W. Molecular characterization of the lincomycin-production gene cluster of Streptomyces lincolnensis 78–11. Mol Microbiol. 1995;16:1137–1156. doi: 10.1111/j.1365-2958.1995.tb02338.x. PubMed DOI

Koberska M, Kopecky J, Olsovska J, Jelinkova M, Ulanova D, Man P, et al. Sequence analysis and heterologous expression of the lincomycin biosynthetic cluster of the type strain Streptomyces lincolnensis ATCC 25466. Folia Microbiol. 2008;53:395–401. doi: 10.1007/s12223-008-0060-8. PubMed DOI

Kamimiya S, Weisblum B. Translational attenuation control of ermSF, an inducible resistance determinant encoding rRNA N-methyltransferase from Streptomyces fradiae. J Bacteriol. 1988;170:1800–1811. PubMed PMC

Gandecha AR, Cundliffe E. Molecular analysis of tlrD, an MLS resistance determinant from the tylosin producer, Streptomyces fradiae. Gene. 1996;180:173–176. doi: 10.1016/S0378-1119(96)00448-9. PubMed DOI

Pernodet JL, Gourmelen A, Blondelet-Rouault MH, Cundliffe E. Dispensable ribosomal resistance to spiramycin conferred by srmA in the spiramycin producer Streptomyces ambofaciens. Microbiology (Reading, Engl) 1999;145:2355–2364. PubMed

Sagova-Mareckova M, Omelka M, Cermak L, Kamenik Z, Olsovska J, Hackl E, et al. Microbial communities show parallels at sites with distinct litter and soil characteristics. Appl Environ Microbiol. 2011;77:7560–7567. doi: 10.1128/AEM.00527-11. PubMed DOI PMC

Schlatter D, Fubuh A, Xiao K, Hernandez D, Kinkel L. Resource amendments influence density and competitive phenotypes of streptomyces in soil. Microb Ecol. 2009;57:413–420. doi: 10.1007/s00248-008-9433-4. PubMed DOI

Bredholdt H, Galatenko OA, Engelhardt K, Fjaervik E, Terekhova LP, Zotchev SB. Rare actinomycete bacteria from the shallow water sediments of the Trondheim fjord, Norway: isolation, diversity and biological activity. Environ Microbiol. 2007;9:2756–2764. doi: 10.1111/j.1462-2920.2007.01387.x. PubMed DOI

Cermak L, Kopecky J, Novotna J, Omelka M, Parkhomenko N, Plhackova K, et al. Bacterial communities of two contrasting soils reacted differently to lincomycin treatment. Appl Soil Ecol. 2008;40:348–358. doi: 10.1016/j.apsoil.2008.06.001. DOI

Ashelford KE, Weightman AJ, Fry JC. PRIMROSE: a computer program for generating and estimating the phylogenetic range of 16S rRNA oligonucleotide probes and primers in conjunction with the RDP-II database. Nucleic Acids Res. 2002;30:3481–3489. doi: 10.1093/nar/gkf450. PubMed DOI PMC

Sakai M, Matsuka A, Komura T, Kanazawa S. Application of a new PCR primer for terminal restriction fragment length polymorphism analysis of the bacterial communities in plant roots. J Microbiol Methods. 2004;59:81–89. doi: 10.1016/j.mimet.2004.06.005. PubMed DOI

Gathogo EWN, Waugh ACW, Peric N, Redpath MB, Long PF. Colony PCR amplification of actinomycete DNA. J Antibiot. 2003;56:423–424. doi: 10.7164/antibiotics.56.423. PubMed DOI

Farnet CM, Staffa A, Yang X. Genes and proteins for the biosynthesis of rosaramicin. Patent 2003; WO 03010193-A2.

Pan Y, Yang X, Li J, Zhang R, Hu Y, Zhou Y, et al. Genome sequence of the spinosyns-producing bacterium Saccharopolyspora spinosa NRRL 18395. J Bacteriol. 2011;193:3150–3151. doi: 10.1128/JB.00344-11. PubMed DOI PMC

Nash KA, Zhang Y, Brown-Elliott BA, Wallace RJ., Jr Molecular basis of intrinsic macrolide resistance in clinical isolates of Mycobacterium fortuitum. J Antimicrob Chemother. 2005;55:170–177. doi: 10.1093/jac/dkh523. PubMed DOI PMC

Zoropogui A, Pujic P, Normand P, Barbe V, Beaman B, Beaman L, et al. Genome sequence of the human- and animal-pathogenic strain Nocardia cyriacigeorgica GUH-2. J Bacteriol. 2012;194:2098–2099. doi: 10.1128/JB.00161-12. PubMed DOI PMC

Roberts AN, Hudson GS, Brenner S. An erythromycin-resistance gene from an erythromycin-producing strain of Arthrobacter sp. Gene. 1985;35:259–270. doi: 10.1016/0378-1119(85)90004-6. PubMed DOI

Doroghazi JR, Ju KS, Brown DW, Labeda DP, Deng Z, Metcalf WW, et al. Genome sequences of three tunicamycin-producing Streptomyces strains, S. chartreusis NRRL 12338, S. chartreusis NRRL 3882, and S. lysosuperificus ATCC 31396. J Bacteriol. 2011;193:7021–7022. doi: 10.1128/JB.06262-11. PubMed DOI PMC

Epp JK, Burgett SG, Schoner BE. Cloning and nucleotide sequence of a carbomycin-resistance gene from Streptomyces thermotolerans. Gene. 1987;53:73–83. doi: 10.1016/0378-1119(87)90094-1. PubMed DOI

Mido N, Hoshigo S, Murakami T. Midecamycin biosynthetic gene cluster. Patent 2004; JP 2004049100-A1.

Xue Y, Zhao L, Liu HW, Sherman DH. A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: architecture of metabolic diversity. Proc Natl Acad Sci U S A. 1998;95:12111–12116. doi: 10.1073/pnas.95.21.12111. PubMed DOI PMC

Mendez C, Salas JA. The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Res Microbiol. 2001;152:341–350. doi: 10.1016/S0923-2508(01)01205-0. PubMed DOI

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Felsenstein J. PHYLIP-Phylogeny inference package (version 3.2) Cladistics. 1989;5:164–166.

Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27:1164–1165. doi: 10.1093/bioinformatics/btr088. PubMed DOI PMC

Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 2001;18:691–699. doi: 10.1093/oxfordjournals.molbev.a003851. PubMed DOI

Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25:1307–1320. doi: 10.1093/molbev/msn067. PubMed DOI

Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25:2286–2288. doi: 10.1093/bioinformatics/btp368. PubMed DOI

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Omelka M, Hudecova S. A comparison of the Mantel test with a generalised distance covariance test. Environmetrics. 2013;24:449–460. doi: 10.1002/env.2238. DOI

Szekely GJ, Rizzo ML, Bakirov NK. Measuring and testing independence by correlation of distances. Ann Stat. 2007;35:2769–2794. doi: 10.1214/009053607000000505. DOI

Baltz RH, Miao V, Wrigley SK. Natural products to drugs: daptomycin and related lipopeptide antibiotics. Nat Prod Rep. 2005;22:717–741. doi: 10.1039/b416648p. PubMed DOI

Egan S, Wiener P, Kallifidas D, Wellington EMH. Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters. Antonie Van Leeuwenhoek. 2001;79:127–133. doi: 10.1023/A:1010296220929. PubMed DOI

Doroghazi JR, Buckley DH. Widespread homologous recombination within and between Streptomyces species. ISME J. 2010;4:1136–1143. doi: 10.1038/ismej.2010.45. PubMed DOI

Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science. 2007;315:476–480. doi: 10.1126/science.1127573. PubMed DOI PMC

Davelos AL, Kinkel LL, Samac DA. Spatial variation in frequency and intensity of antibiotic interactions among streptomycetes from prairie soil. Appl Environ Microbiol. 2004;70:1051–1058. doi: 10.1128/AEM.70.2.1051-1058.2004. PubMed DOI PMC

Fischbach MA, Walsh CT, Clardy J. The evolution of gene collectives: How natural selection drives chemical innovation. Proc Natl Acad Sci U S A. 2008;105:4601–4608. doi: 10.1073/pnas.0709132105. PubMed DOI PMC

Gonzalez I, Niebla A, Lemus M, Gonzalez L, Iznaga IO, Perez ME, et al. Ecological approach of macrolide-lincosamides-streptogramin producing Actinomyces from Cuban soils. Lett Appl Microbiol. 1999;29:147–150. doi: 10.1046/j.1365-2672.1999.00580.x. PubMed DOI

Kopecky J, Kyselkova M, Omelka M, Cermak L, Novotna J, Grundmann GL, et al. Actinobacterial community dominated by a distinct clade in acidic soil of a waterlogged deciduous forest. FEMS Microbiol Ecol. 2011;78:386–394. doi: 10.1111/j.1574-6941.2011.01173.x. PubMed DOI

Jensen PR. Linking species concepts to natural product discovery in the post-genomic era. J Ind Microbiol Biotechnol. 2010;37:219–224. doi: 10.1007/s10295-009-0683-z. PubMed DOI PMC

Zakalyukina YV, Zenova GM. Antagonistic activity of soil acidophilic actinomycetes. Biol Bull. 2007;34:329–332. doi: 10.1134/S1062359007040036. PubMed DOI

Comparison of Actinobacteria communities from human-impacted and pristine karst caves

See more in PubMed

GENBANK
KF960851, KF960852, KF960853, KF960854, KF960855, KF960856, KF960857, KF960858, KF960859, KF960860, KF960861, KF960862, KF960863, KF960864, KF960865, KF960866, KF960867, KF960868, KF960869, KF960870, KF960871, KF960872, KF960873, KF960874, KF960875, KF960876, KF960877, KF960878, KF960879, KF960880, KF960881, KF960882, KF960883, KF960884, KF960885, KF960886, KF960887, KF960888, KF960889, KF960890, KF960891, KF960892, KF960893, KF960894, KF960895, KF960896, KF960897, KF960898, KF960899, KF960900, KF960901, KF960902, KF960903, KF960904, KF960905, KF960906, KF960907, KF960908, KF960909, KF960910, KF960911, KF960912, KF960913, KF960914, KF960915, KF960916, KF960917, KF960918, KF960919, KF960920, KF960921, KF960922, KF960923, KF960924, KF960925, KF960926, KF960927, KF960928, KF960929, KF960930, KF960931, KF960932, KF960933, KF960934, KF960935, KF960936, KF960937, KF960938, KF960939, KF960940, KF960941, KF960942, KF960943, KF960944, KF960945, KF960946, KF960947, KF960948, KF960949, KF960950, KF960951, KF960952, KF960953, KF960954, KF960955, KF960956, KF960957, KF960958, KF960959, KF960960, KF960961, KF960962, KF960963, KF960964