Field-based evidence for consistent responses of bacterial communities to copper contamination in two contrasting agricultural soils

Copper contamination on China's arable land could pose severe economic, ecological and healthy consequences in the coming decades. As the drivers in maintaining ecosystem functioning, the responses of soil microorganisms to long-term copper contamination in different soil ecosystems are still debated. This study investigated the impacts of copper gradients on soil bacterial communities in two agricultural fields with contrasting soil properties. Our results revealed consistent reduction in soil microbial biomass carbon (SMBC) with increasing copper levels in both soils, coupled by significant declines in bacterial abundance in most cases. Despite of contrasting bacterial community structures between the two soils, the bacterial diversity in the copper-contaminated soils showed considerably decreasing patterns when copper levels elevated. High-throughput sequencing revealed copper selection for major bacterial guilds, in particular, Actinobacteria showed tolerance, while Acidobacteria and Chloroflexi were highly sensitive to copper. The thresholds that bacterial communities changed sharply were 800 and 200 added copper mg kg−1 in the fluvo-aquic soil and red soil, respectively, which were similar to the toxicity thresholds (EC50 values) characterized by SMBC. Structural equation model (SEM) analysis ascertained that the shifts of bacterial community composition and diversity were closely related with the changes of SMBC in both soils. Our results provide field-based evidence that copper contamination exhibits consistently negative impacts on soil bacterial communities, and the shifts of bacterial communities could have largely determined the variations of the microbial biomass.

[1]  Christopher Quince,et al.  Loss of microbial diversity in soils is coincident with reductions in some specialized functions. , 2014, Environmental microbiology.

[2]  S. Soni,et al.  Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations , 2014, The ISME Journal.

[3]  M. V. D. van der Heijden,et al.  Soil biodiversity and soil community composition determine ecosystem multifunctionality , 2014, Proceedings of the National Academy of Sciences.

[4]  Yuan-ming Zheng,et al.  Initial Copper Stress Strengthens the Resistance of Soil Microorganisms to a Subsequent Copper Stress , 2014, Microbial Ecology.

[5]  Zongwei Ma,et al.  A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. , 2014, The Science of the total environment.

[6]  B. Singh,et al.  Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. , 2013, Trends in microbiology.

[7]  Rob Knight,et al.  Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States , 2013, Science.

[8]  Brian C. Thomas,et al.  Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling , 2013, Microbiome.

[9]  Yu Dai,et al.  pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing , 2013, Journal of Soils and Sediments.

[10]  Mark V Brown,et al.  Microbial community responses to anthropogenically induced environmental change: towards a systems approach. , 2013, Ecology letters.

[11]  B. Griffiths,et al.  Insights into the resistance and resilience of the soil microbial community. , 2013, FEMS microbiology reviews.

[12]  M. Chodak,et al.  Diversity of microorganisms from forest soils differently polluted with heavy metals , 2013 .

[13]  Michel Loreau,et al.  Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. , 2013, Ecology letters.

[14]  J. Ravel,et al.  Microbiome, demystifying the role of microbial communities in the biosphere , 2013, Microbiome.

[15]  Ji‐Zheng He,et al.  Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils , 2012 .

[16]  Didier L. Baho,et al.  Fundamentals of Microbial Community Resistance and Resilience , 2012, Front. Microbio..

[17]  B. Singh,et al.  Long-term impacts of zinc and copper enriched sewage sludge additions on bacterial, archaeal and fungal communities in arable and grassland soils , 2011 .

[18]  Rob Knight,et al.  Examining the global distribution of dominant archaeal populations in soil , 2011, The ISME Journal.

[19]  Robert C. Edgar,et al.  Search and clustering orders of magnitude faster than BLAST , 2010, Bioinform..

[20]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[21]  O. Nybroe,et al.  Development of pollution-induced community tolerance is linked to structural and functional resilience of a soil bacterial community following a five-year field exposure to copper , 2010 .

[22]  M. Mclaughlin,et al.  Influences of soil properties and leaching on copper toxicity to barley root elongation , 2010, Environmental toxicology and chemistry.

[23]  Y. Ma,et al.  Toxicity and accumulation of copper and nickel in maize plants cropped on calcareous and acidic field soils , 2010, Plant and Soil.

[24]  M. Mclaughlin,et al.  A single application of Cu to field soil has long-term effects on bacterial community structure, diversity, and soil processes. , 2010 .

[25]  E. Zavaleta,et al.  Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity , 2010, Proceedings of the National Academy of Sciences.

[26]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[27]  K. Giller,et al.  Heavy metals and soil microbes , 2009 .

[28]  W. Verstraete,et al.  Initial community evenness favours functionality under selective stress , 2009, Nature.

[29]  M. McBride,et al.  Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. , 2009, The Science of the total environment.

[30]  R. Knight,et al.  A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses , 2009, The ISME Journal.

[31]  B. Singh,et al.  Multiple profiling of soil microbial communities identifies potential genetic markers of metal-enriched sewage sludge. , 2008, FEMS microbiology ecology.

[32]  L. Ranjard,et al.  Copper dynamics and impact on microbial communities in soils of variable organic status. , 2008, Environmental science & technology.

[33]  E. Kothe,et al.  Microbes and metals: interactions in the environment , 2007, Journal of basic microbiology.

[34]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[35]  I. Oliver,et al.  Long-term aging of copper added to soils. , 2006, Environmental science & technology.

[36]  James B. Grace,et al.  Structural Equation Modeling and Natural Systems , 2006 .

[37]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[38]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  W. Ludwig,et al.  Detection and Phylogenetic Relationships of Highly Diverse Uncultured Acidobacterial Communities in Altamira Cave Using 23S rRNA Sequence Analyses , 2005 .

[40]  J. Prosser,et al.  Bacterial diversity promotes community stability and functional resilience after perturbation. , 2005, Environmental microbiology.

[41]  D. Mcphail,et al.  Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia , 2004 .

[42]  E. Delong,et al.  Quantitative Analysis of Small-Subunit rRNA Genes in Mixed Microbial Populations via 5′-Nuclease Assays , 2000, Applied and Environmental Microbiology.

[43]  Yaocheng Fan,et al.  HEAVY METAL CONTAMINATION IN VEGETABLES AND THEIR CONTROL IN CHINA , 2000 .

[44]  Ken E. Giller,et al.  Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review , 1998 .

[45]  M. K. Holland.  TOXICITY OF HEAVY METALS , 1979 .

[46]  L. Jackson,et al.  Land use and climatic factors structure regional patterns in soil microbial communities. , 2010, Global ecology and biogeography : a journal of macroecology.

[47]  Meng Qian,et al.  Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. , 2010, Bioresource technology.

[48]  R. Gilkes,et al.  Copper dynamics and impact on microbial communities in a vineyard soil. Influence of the soil organic status. , 2010 .

[49]  Stephen R. Smith,et al.  A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge. , 2009, Environment international.

[50]  D. Mcphail,et al.  COPPER ACCUMULATION DISTRIBUTION AND FRACTIONATION IN VINEYARD SOIL OF VICTORIA , 2004 .

[51]  Jinshui Wu,et al.  Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure , 1990 .

[52]  J. R.,et al.  Quantitative analysis , 1892, Nature.