Reconstructing rare soil microbial genomes using in situ enrichments and metagenomics

Frontiers in Microbiology

Volumn 6, Issue APR, 2015, Pages

  Delmont, Tom O ^a,b   Eren, A Murat ^b   Maccario, Lorrie ^a   Prestat, Emmanuel ^a   Esen, Özcan C ^b   Pelletier, Eric ^c,d,e   Le Paslier, Denis ^c,d,e   Simonet, Pascal ^a   Vogel, Timothy M ^a  

^a ECOLE CENTRALE DE LYON   (France)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^d CNRS   (France)

^e UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

Author keywords

Environmental genomics; Metagenomics; Phages; Plasmids; Rare biosphere; Soil

Indexed keywords

HEAVY METAL;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BURKHOLDERIA; CONTROLLED STUDY; ENRICHMENT CULTURE; GENE AMPLIFICATION; GENE SEQUENCE; GENETIC VARIABILITY; METAGENOMICS; MICROCOSM; NITROGEN FIXATION; NONHUMAN; PYROSEQUENCING; SOIL MICROFLORA; STREPTOMYCES; TAXONOMY;

ACIDOBACTERIA; BACTERIA (MICROORGANISMS); BURKHOLDERIA; LEIFSONIA; RHODANOBACTER; SPOROLACTOBACILLUS; STREPTOMYCES;

EID: 84930943953     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00358     Document Type: Article

References (66)

1. Albertsen, M., Hugenholtz, P., Skarshewski, A., Nielsen, K. L., Tyson, G. W., and Nielsen, P. H. (2013). Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533-538. doi: 10.1038/nbt.2579.
2. Anantharaman, K., Breier, J. A., Sheik, C. S., and Dick, G. J. (2013). Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. U.S.A. 110, 330-335. doi: 10.1073/pnas.1215340110.
3. Andersson, D. I., and Hughes, D. (2010). Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8, 260-271. doi: 10.1038/nrmicro2319.
4. Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., et al. (2008). The RAST Server: rapid annotations using subsystems technology. BMC genomics 9:75. doi: 10.1186/1471-2164-9-75.
5. Barrineau, P., Gilbert, P., Jackson, W., Jones, C., Summers, A., and Wisdom, S. (1983). The DNA sequence of the mercury resistance operon of the IncFII plasmid NR1. J. Mol. Appl. Genet. 2, 601-619.
6. Bastian, M., Heymann, S., and Jacomy, M. (2009). Gephi: an open source software for exploring and manipulating networks. ICWSM 8, 361-362.
7. Bothe, H., Ferguson, S., and Newton, W. E. (2006). Biology of the Nitrogen Cycle. Amsterdam: Elsevier.
8. Boubakri, H., Beuf, M., Simonet, P., and Vogel, T. M. (2006). Development of metagenomic DNA shuffling for the construction of a xenobiotic gene. Gene 375, 87-94. doi: 10.1016/j.gene.2006.02.027.
9. Carver, T., Thomson, N., Bleasby, A., Berriman, M., and Parkhill, J. (2009). DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25, 119-120. doi: 10.1093/bioinformatics/btn578.
10. Chain, P. S., Denef, V. J., Konstantinidis, K. T., Vergez, L. M., Agulló, L., Reyes, V. L., et al. (2006). Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc. Natl. Acad. Sci. U.S.A. 103, 15280-15287. doi: 10.1073/pnas.0606924103.
11. Chang, Y.-J., Land, M., Hauser, L., Chertkov, O., Del Rio, T. G., Nolan, M., et al. (2011). Non-contiguous finished genome sequence and contextual data of the filamentous soil bacterium Ktedonobacter racemifer type strain (SOSP1-21T). Stand. Genomic Sci. 5, 97. doi: 10.4056/sigs.2114901.
12. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., et al. (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141-D145. doi: 10.1093/nar/gkn879.
13. Daniel, R. (2004). The soil metagenome-a rich resource for the discovery of novel natural products. Curr. Opin. Biotechnol. 15, 199-204. doi: 10.1016/j.copbio.2004.04.005.
14. David, M. M., Cecillon, S., Warne, B. M., Prestat, E., Jansson, J. K., and Vogel, T. M. (2014). Microbial ecology of chlorinated solvent biodegradation. Environ. Microbiol. doi: 10.1111/1462-2920.12413. [Epub ahead of print].
15. Delmont, T. O., Francioli, D., Jacquesson, S., Laoudi, S., Mathieu, A., Nesme, J., et al. (2014). Microbial community development and unseen diversity recovery in inoculated sterile soil. Biol. Fertil. Soils 50, 1069-1076. doi: 10.1007/s00374-014-0925-8.
16. Delmont, T. O., Malandain, C., Prestat, E., Larose, C., Monier, J. M., Simonet, P., et al. (2011a). Metagenomic mining for microbiologists. ISME J. 5, 1837-1843. doi: 10.1038/ismej.2011.61.
17. Delmont, T. O., Prestat, E., Keegan, K. P., Faubladier, M., Robe, P., Clark, I. M., et al. (2012). Structure, fluctuation and magnitude of a natural grassland soil metagenome. ISME J. 6, 1677-1687. doi: 10.1038/ismej.2011.197.
18. Delmont, T. O., Robe, P., Cecillon, S., Clark, I. M., Constancias, F., Simonet, P., et al. (2011b). Accessing the soil metagenome for studies of microbial diversity. Appl. Environ. Microbiol. 77, 1315-1324. doi: 10.1128/AEM.01526-10.
19. Falkowski, P., Scholes, R., Boyle, E., Canadell, J., Canfield, D., Elser, J., et al. (2000). The global carbon cycle: a test of our knowledge of earth as a system. Science 290, 291-296. doi: 10.1126/science.290.5490.291.
20. Fierer, N., Leff, J. W., Adams, B. J., Nielsen, U. N., Bates, S. T., Lauber, C. L., et al. (2012). Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc. Natl. Acad. Sci. U.S.A. 109, 21390-21395. doi: 10.1073/pnas.1215210110.
21. Finzi, A. C., Austin, A. T., Cleland, E. E., Frey, S. D., Houlton, B. Z., and Wallenstein, M. D. (2011). Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front. Ecol. Environ. 9, 61-67. doi: 10.1890/100001.
22. Galvão, T. C., Mohn, W. W., and de Lorenzo, V. (2005). Exploring the microbial biodegradation and biotransformation gene pool. Trends Biotechnol. 23, 497-506. doi: 10.1016/j.tibtech.2005.08.002.
23. Gans, J., Wolinsky, M., and Dunbar, J. (2005). Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309, 1387-1390. doi: 10.1126/science.1112665.
24. Garcia Martin, H., Ivanova, N., Kunin, V., Warnecke, F., Barry, K. W., McHardy, A. C., et al. (2006). Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities. Nat. Biotechnol. 24, 1263-1269. doi: 10.1038/nbt1247.
25. Giller, K., Beare, M., Lavelle, P., Izac, A., and Swift, M. (1997). Agricultural intensification, soil biodiversity and agroecosystem function. Appl. Soil Ecol. 6, 3-16. doi: 10.1016/S0929-1393(96)00149-7.
26. Green, S. J., Prakash, O., Jasrotia, P., Overholt, W. A., Cardenas, E., Hubbard, D., et al. (2012). Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. Appl. Environ. Microbiol. 78, 1039-1047. doi: 10.1128/AEM.06435-11.
27. Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J., and Goodman, R. M. (1998). Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5, R245-249. doi: 10.1016/S1074-5521(98)90108-9.
28. Hess, M., Sczyrba, A., Egan, R., Kim, T. W., Chokhawala, H., Schroth, G., et al. (2011). Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331, 463-467. doi: 10.1126/science.1200387.
29. Howe, A. C., Jansson, J. K., Malfatti, S. A., Tringe, S. G., Tiedje, J. M., and Brown, C. T. (2014). Tackling soil diversity with the assembly of large, complex metagenomes. Proc. Natl. Acad. Sci. U.S.A. 111, 4904-4909. doi: 10.1073/pnas.1402564111.
30. Ibekwe, A., Papiernik, S., Gan, J., Yates, S., Crowley, D., and Yang, C. H. (2001). Microcosm enrichment of 1, 3-dichloropropene-degrading soil microbial communities in a compost-amended soil. J. Appl. Microbiol. 91, 668-676. doi: 10.1046/j.1365-2672.2001.01431.x.
31. Jacquiod, S., Franqueville, L., Cécillon, S., Vogel, T. M., and Simonet, P. (2013). Soil bacterial community shifts after chitin enrichment: an integrative metagenomic approach. PLoS ONE 8:e79699. doi: 10.1371/journal.pone.0079699.
32. Jaspers, E., and Overmann, J. (2004). Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl. Environ. Microbiol. 70, 4831-4839. doi: 10.1128/AEM.70.8.4831-4839.2004.
33. Kennedy, A., and Smith, K. (1995). Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170, 75-86. doi: 10.1007/BF02183056.
34. Kostka, J. E., Green, S. J., Rishishwar, L., Prakash, O., Katz, L. S., Mariño-Ramírez, L., et al. (2012). Genome sequences for six Rhodanobacter strains, isolated from soils and the terrestrial subsurface, with variable denitrification capabilities. J. Bacteriol. 194, 4461-4462. doi: 10.1128/JB.00871-12.
35. Lin, L. L., Schneider, T., Peoples, A. J., Spoering, A. L., Engels, I., Conlon, B. P., et al. (2015). A new antibiotic kills pathogens without detectable resistance. Nature 517, 455-459. doi: 10.1038/nature14098.
36. Liu, Z., Klatt, C. G., Ludwig, M., Rusch, D. B., Jensen, S. I., Kühl, M., et al. (2012). 'Candidatus Thermochlorobacter aerophilum:'an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME J. 6, 1869-1882. doi: 10.1038/ismej.2012.24.
37. Luo, C., Tsementzi, D., Kyrpides, N. C., and Konstantinidis, K. T. (2012). Individual genome assembly from complex community short-read metagenomic datasets. ISME J. 6, 898-901. doi: 10.1038/ismej.2011.147.
38. Mackelprang, R., Waldrop, M. P., DeAngelis, K. M., David, M. M., Chavarria, K. L., Blazewicz, S. J., et al. (2011). Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368-371. doi: 10.1038/nature10576.
39. Malpartida, F., and Hopwood, D. (1984). Molecular cloning of the whole biosynthetic pathway of a Streptomyces antibiotic and its expression in a heterologous host. Nature 309, 462-464.
40. Martinez, J., and Baquero, F. (2000). Mutation frequencies and antibiotic resistance. Antimicrob. Agents Chemother. 44, 1771-1777. doi: 10.1128/AAC.44.7.1771-1777.2000.
41. McIlroy, S. J., Albertsen, M., Andresen, E. K., Saunders, A. M., Kristiansen, R., Stokholm-Bjerregaard, M., et al. (2013). 'Candidatus Competibacter'-lineage genomes retrieved from metagenomes reveal functional metabolic diversity. ISME J. 8, 613-624. doi: 10.1038/ismej.2013.162.
42. McKew, B. A., Coulon, F., Osborn, A. M., Timmis, K. N., and McGenity, T. J. (2007). Determining the identity and roles of oil-metabolizing marine bacteria from the Thames Estuary, UK. Environ. Microbiol. 9, 165-176. doi: 10.1111/j.1462-2920.2006.01125.x.
43. Mende, D. R., Waller, A. S., Sunagawa, S., Järvelin, A. I., Chan, M. M., Arumugam, M., et al. (2012). Assessment of metagenomic assembly using simulated next generation sequencing data. PLoS ONE 7:e31386. doi: 10.1371/journal.pone.0031386.
44. Meyer, F., Paarmann, D., D'Souza, M., Olson, R., Glass, E. M., Kubal, M., et al. (2008). The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi: 10.1186/1471-2105-9-386.
45. Narasingarao, P., Podell, S., Ugalde, J. A., Brochier-Armanet, C., Emerson, J. B., Brocks, J. J., et al. (2012). De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81-93. doi: 10.1038/ismej.2011.78.
46. Nesme, J., Cécillon, S., Delmont, T. O., Monier, J.-M., Vogel, T. M., and Simonet, P. (2014). Large-scale metagenomic-based study of antibiotic resistance in the environment. Curr. Biol. 24, 1096-1100. doi: 10.1016/j.cub.2014.03.036.
47. Nielsen, H. B., Almeida, M., Juncker, A. S., Rasmussen, S., Li, J., Sunagawa, S., et al. (2014). Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822-828. doi: 10.1038/nbt.2939.
48. Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M. H. H., Oksanen, M. J., et al. (2007). The Vegan Package. Community ecology package.
49. Osborn, A. M., Bruce, K. D., Strike, P., and Ritchie, D. A. (1997). Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol. Rev. 19, 239-262. doi: 10.1111/j.1574-6976.1997.tb00300.x.
50. Pell, J., Hintze, A., Canino-Koning, R., Howe, A., Tiedje, J. M., and Brown, C. T. (2012). Scaling metagenome sequence assembly with probabilistic de Bruijn graphs. Proc. Natl. Acad. Sci. U.S.A. 109, 13272-13277. doi: 10.1073/pnas.1121464109.
51. Pena, A., Teeling, H., Huerta-Cepas, J., Santos, F., Yarza, P., Brito-Echeverría, J., et al. (2010). Fine-scale evolution: genomic, phenotypic and ecological differentiation in two coexisting Salinibacter ruber strains. ISME J. 4, 882-895. doi: 10.1038/ismej.2010.6.
52. Peoples, M., Herridge, D., and Ladha, J. (1995). Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174, 3-28. doi: 10.1007/BF00032239.
53. Prosser, J. I., Rangel-Castro, J. I., and Killham, K. (2006). Studying plant-microbe interactions using stable isotope technologies. Curr. Opin. Biotechnol. 17, 98-102. doi: 10.1016/j.copbio.2006.01.001.
54. Roesch, L. F., Fulthorpe, R. R., Riva, A., Casella, G., Hadwin, A. K., Kent, A. D., et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1, 283-290. doi: 10.1038/ismej.2007.53.
55. Rondon, M. R., August, P. R., Bettermann, A. D., Brady, S. F., Grossman, T. H., Liles, M. R., et al. (2000). Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66, 2541-2547. doi: 10.1128/AEM.66.6.2541-2547.2000.
56. Sharon, I., Morowitz, M. J., Thomas, B. C., Costello, E. K., Relman, D. A., and Banfield, J. F. (2013). Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res. 23, 111-120. doi: 10.1101/gr.142315.112.
57. Stahl, D. A., Lane, D. J., Olsen, G. J., and Pace, N. R. (1984). Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science 224: 409-411. doi: 10.1126/science.224.4647.409.
58. Thomson, C. J. (1999). The global epidemiology of resistance to ciprofloxacin and the changing nature of antibiotic resistance: a 10 year perspective. J. Antimicrob. Chemother. 43, 31-40. doi: 10.1093/jac/43.suppl_1.31.
59. Torsvik, V., Ovreas, L., and Thingstad, T. F. (2002). Prokaryotic diversity-magnitude, dynamics, and controlling factors. Science 296, 1064-1066. doi: 10.1126/science.1071698.
60. Tringe, S. G., von Mering, C., Kobayashi, A., Salamov, A. A., Chen, K., Chang, H. W., et al. (2005). Comparative metagenomics of microbial communities. Science 308, 554-557. doi: 10.1126/science.1107851.
61. Tyson, G. W., Chapman, J., Hugenholtz, P., Allen, E. E., Ram, R. J., Richardson, P. M., et al. (2004). Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37-43. doi: 10.1038/nature02340.
62. Vogel, T. M., Simonet, P., Jansson, J. K., Hirsch, P. R., Tiedje, J. M., Van Elsas, J. D., et al. (2009). TerraGenome: a consortium for the sequencing of a soil metagenome. Nat. Rev. Microbiol. 7, 252. doi: 10.1038/nrmicro2119.
63. Wagner-Döbler, I., Bennasar, A., Vancanneyt, M., Strömpl, C., Brümmer, I., Eichner, C., et al. (1998). Microcosm enrichment of biphenyl-degrading microbial communities from soils and sediments. Appl. Environ. Microbiol. 64, 3014-3022.
64. Wommack, K. E., Bhavsar, J., and Ravel, J. (2008). Metagenomics: read length matters. Appl. Environ. Microbiol. 74, 1453-1463. doi: 10.1128/AEM.02181-07.
65. Wu, M., and Eisen, J. A. (2008). A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9:R151. doi: 10.1186/gb-2008-9-10-r151.
66. Yakimov, M. M., Denaro, R., Genovese, M., Cappello, S., D'Auria, G., Chernikova, T. N., et al. (2005). Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ. Microbiol. 7, 1426-1441. doi: 10.1111/j.1462-5822.2005.00829.x.