Abstract
We performed a longitudinal study (repeated observations of the same sample over time) to investigate both the composition and structure of temporal changes of bacterial community composition in soil mesocosms, subjected to three different treatments (water and 5 or 25 mg kg−1 of dried soil Cd2+). By analogy with the pan genome concept, we identified a core bacteriome and an accessory bacteriome. Resident taxa were assigned to the core bacteriome, while occasional taxa were assigned to the accessory bacteriome. Core and accessory bacteriome represented roughly 35 and 50 % of the taxa detected, respectively, and were characterized by different taxonomic signatures from phylum to genus level while 15 % of the taxa were found to be unique to a particular sample. In particular, the core bacteriome was characterized by higher abundance of members of Planctomycetes, Actinobacteria, Verrucomicrobia and Acidobacteria, while the accessory bacteriome included more members of Firmicutes, Clamydiae and Proteobacteria, suggesting potentially different responses to environmental changes of members from these phyla. We conclude that the pan-bacteriome model may be a useful approach to gain insight for modeling bacterial community structure and inferring different abilities of bacteria taxa.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105:11512–11519. doi:10.1073/pnas.0801925105
Aravindraja C, Viszwapriya D, Karutha Pandian S (2013) Ultradeep 16S rRNA sequencing analysis of geographically similar but diverse unexplored marine samples reveal varied bacterial community composition. PLoS One 8:e76724
Ascher J et al (2009) Sequential extraction and genetic fingerprinting of a forest soil metagenome. Appl Soil Ecol 42:176–181. doi:10.1016/j.apsoil.2009.03.005
Bacci G, Bazzicalupo M, Benedetti A, Mengoni A (2014) StreamingTrim 1.0: a Java software for dynamic trimming of 16S rRNA sequence data from metagenetic studies. Mol Ecol Resour 14:426–434. doi:10.1111/1755-0998.12187
Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol 77:3846–3852. doi:10.1128/aem.02772-10
Bartram AK, Jiang X, Lynch MD, Masella AP, Nicol GW, Dushoff J, Neufeld JD (2014) Exploring links between pH and bacterial community composition in soils from the Craibstone Experimental Farm. FEMS Microbiol Ecol 87:403–415
Bowen JL, Morrison HG, Hobbie JE, Sogin ML (2012) Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. ISME J 6:2014–2023
Campbell BJ, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci USA 108:12776–12781. doi:10.1073/pnas.1101405108
Ceccherini M, Ascher J, Pietramellara G, Mocali S, Viti C, Nannipieri P (2007) The effect of pharmaceutical waste-fungal biomass, treated to degrade DNA, on the composition of eubacterial and ammonia oxidizing populations of soil. Biol Fertil Soils 44:299–306. doi:10.1007/s00374-007-0204-z
Chaparro J, Sheflin A, Manter D, Vivanco J (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499. doi:10.1007/s00374-012-0691-4
Chien C, Kuo Y, Chen C, Hung C, Yeh C, Yeh W (2008) Microbial diversity of soil bacteria in agricultural field contaminated with heavy metals. J Environ Sci 20:359–363
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697
Dineen SM, Aranda R, Anders DL, Robertson JM (2010) An evaluation of commercial DNA extraction kits for the isolation of bacterial spore DNA from soil. J Appl Microbiol 109:1886–1896. doi:10.1111/j.1365-2672.2010.04816.x
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930
Dohrmann AB, Küting M, Jünemann S, Jaenicke S, Schlüter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt-and conventional maize varieties. ISME J 7:37–49
Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt M (2014) Evolution of bacterial communities in the wheat crop rhizosphere. Environ Microbiol. doi:10.1111/1462-2920.12452
Duan X, Huang C (2008) Effect of cadmium on diversity of microbial genes in paddy soil. Chin J Appl Environ Biol 14:510–513
Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred II. Error probabilities. Genome Res 8:186–194
Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred I. Accuracy assessment. Genome Res 8:175–185
Fritze H et al (2000) Effect of Cd-containing wood ash on the microflora of coniferous forest humus. Fems Microbiol Ecol 32:43–51
Ge Y, He J-Z, Zhu Y-G, Zhang J-B, Xu Z, Zhang L-M, Zheng Y-M (2008) Differences in soil bacterial diversity: driven by contemporary disturbances or historical contingencies? ISME J 2:254–264
Gibbons SM, Caporaso JG, Pirrung M, Field D, Knight R, Gilbert JA (2013) Evidence for a persistent microbial seed bank throughout the global ocean. Proc Natl Acad Sci USA 110:4651–4655
Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, MacPhee R, Reid G (2010) Microbiome profiling by illumina sequencing of combinatorial sequence-tagged PCR products. PLoS One 5:e15406
Gobet A et al (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 6:542–553
Gomes NCM, Landi L, Smalla K, Nannipieri P, Brookes PC, Renella G (2010) Effects of Cd- and Zn-enriched sewage sludge on soil bacterial and fungal communities. Ecotoxicol Environ Saf 73:1255–1263
Hardoim CCP, Costa R (2014) Temporal dynamics of prokaryotic communities in the marine sponge Sarcotragus spinosulus. Mol Ecol 23:3097–3112. doi:10.1111/mec.12789
Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255
Kim TS, Jeong JY, Wells GF, Park HD (2013) General and rare bacterial taxa demonstrating different temporal dynamic patterns in an activated sludge bioreactor. Appl Microbiol Biotechnol 97:1755–1765
Kuang J-L et al (2012) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 7:1038–1050
Lazzaro A, Widmer F, Sperisen C, Frey B (2008) Identification of dominant bacterial phylotypes in a cadmium-treated forest soil. FEMS Microbiol Ecol 63:143–155
Logares R et al (2013) Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J 7:937–948
Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P, Kandeler E (2006) Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biol Biochem 38:1430–1437
L-X Chen, J-T Li, Y-T Chen, L-N Huang, Z-S Hua, Hu M, Shu W-S (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15:2431–2444. doi:10.1111/1462-2920.12114
Masella A, Bartram A, Truszkowski J, Brown D, Neufeld J (2012) PANDAseq: paired-end assembler for illumina sequences. BMC Bioinform 13:31
Mengoni A, Schat H, Vangronsveld J (2010) Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331:5–16
Oh J et al (2013) The altered landscape of the human skin microbiome in patients with primary immunodeficiencies. Genome Res 23:2103–2114
Oksanen J et al. (2013) vegan: community ecology package. R package version 2.0-10. http://vegan.r-forge.r-project.org/
Pedrós-Alió C (2012) The rare bacterial biosphere. Annu Rev Mar Sci 4:449–466. doi:10.1146/annurev-marine-120710-100948
Pini F, Frascella A, Santopolo L, Bazzicalupo M, Biondi E, Scotti C, Mengoni A (2012) Exploring the plant-associated bacterial communities in Medicago sativa L. BMC Microbiol 12:78
Porter SS, Rice KJ (2013) Trade-offs, spatial heterogeneity, and the maintenance of microbial diversity. Evolution 67:599–608
Portillo MC, Leff JW, Lauber CL, Fierer N (2013) Cell size distributions of soil bacterial and archaeal taxa. Appl Environ Microbiol 79:7610–7617
Renella G, Brookes PC, Nannipieri P (2002) Cadmium and zinc toxicity to soil microbial biomass and activity. Dev Soil Sci 28:267–273
Renella G, Mench M, Landi L, Nannipieri P (2005) Microbial activity and hydrolase synthesis in long-term Cd-contaminated soils. Soil Biol Biochem 37:133–139
Safriel UN, Ritte U (1980) Criteria for the identification of potential colonizers. Biol J Linn Soc 13:287–297
Sánchez O, Ferrera I, González JM, Mas J (2013) Assessing bacterial diversity in a seawater-processing wastewater treatment plant by 454-pyrosequencing of the 16S rRNA and amoA genes. Microb Biotechnol 6:435–442
Sheoran V, Sheoran AS, Poonam P (2008) Remediation techniques for contaminated soils. Environ Eng Manag J 7:379–387
Smith BC et al (2012) The cervical microbiome over 7 years and a comparison of methodologies for its characterization. PLoS One 7:e40425
Sogin ML et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120. doi:10.1073/pnas.0605127103
Székely AJ, Langenheder S (2014) The importance of species sorting differs between habitat generalists and specialists in bacterial communities. Fems Microbiol Ecol 87:102–112
Tamaki H et al (2010) Armatimonas rosea gen. nov., sp. nov., of a novel bacterial phylum, Armatimonadetes phyl. nov., formally called the candidate phylum OP10. Int J Syst Evol Microbiol 61:1442–1447. doi:10.1099/ijs.0.025643-0
Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11:472–477
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/aem.00062-07
Wegner KM, Volkenborn N, Peter H, Eiler A (2013) Disturbance induced decoupling between host genetics and composition of the associated microbiome. BMC Microbiol 13:252
Xu XH, Liu CY, Li RY, Wang XR (2013) Impacts of cadmium stress on soil microbial and enzyme activities under laboratory conditions. J Food Agric Environ 11:1730–1734
Zhang Y, Zhang X, Zhang H, He Q, Zhou Q, Su Z, Zhang C (2009) Responses of soil bacteria to long-term and short-term cadmium stress as revealed by microbial community analysis. Bull Environ Contam Toxicol 82:367–372
Zhou J et al (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proc Natl Acad Sci USA 111:E836–E845. doi:10.1073/pnas.1324044111
Acknowledgments
This work was supported by a grant from the Ente Cassa di Risparmio di Firenze (Grant No. 2010/4384 “Centro di Metagenomica del suolo”).
Author information
Authors and Affiliations
Corresponding author
Additional information
Giovanni Bacci and Maria Teresa Ceccherini have equally contributed to the work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bacci, G., Ceccherini, M.T., Bani, A. et al. Exploring the dynamics of bacterial community composition in soil: the pan-bacteriome approach. Antonie van Leeuwenhoek 107, 785–797 (2015). https://doi.org/10.1007/s10482-014-0372-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-014-0372-4