Changes in the microbial community of an arable soil caused by long-term metal contamination

The effects of past applications of farmyard manure (FYM, applied from 1942 to 1967), metal-contaminated sewage sludge (applied from 1942 to 1961) and mineral fertilizer (NPK, applied from 1942 until now) on the microbial biomass and community structure in a sandy loam, arable soil from the Woburn Market Garden Experiment, UK, were investigated in 1998. Concentrations of Cu, Ni and Zn in soils which previously received sewage sludge were less than current European Union (EU) limits, but the soil Cd concentration was more than twice the permitted limit. Organic-C concentration in the FYM-treated soil and contaminated soils was about twice that of NPK-treated soil. The initial microbial biomass-C and estimates of total bacterial numbers by acridine orange direct count were significantly (P < 0.05) greater in the FYM-treated soil compared with the NPK-treated and the most contaminated soils. Total phospholipid fatty acid (PLFA) concentration (another measure of biomass) was significantly greater in the FYM-treated soil compared with either the low or high metal-contaminated soils, both of which contained similar PLFA concentrations. In the metal-contaminated soils, in contrast, fluorescent Pseudomonas counts, as a percentage of total plate counts, were at least 1.5 times greater than in the uncontaminated soils. The concentrations of these microbial parameters were significantly (P < 0.05) less in the NPK soil than in all the other treatments. Biomass-C as a percentage of organic-C was also significantly (P < 0.05) greater in the uncontaminated soils compared with the metal-contaminated soils. Biomass specific respiration rates in the metal-contaminated soils were c. 1.5 times those in the FYM-treated soil. In the metal-contaminated soils, the concentration of mono-unsaturated and hydroxy-fatty acids (derived from phospholipids), and lipopolysaccharide hydroxy-fatty acids (all indicative of Gram-negative bacteria) were significantly (P < 0.05) greater than branched fatty acids (indicative of Gram-positive bacteria). Furthermore, Gram-negative counts were 62-68% greater than Gram-positive counts in the metal-contaminated soils. Branched fatty acid concentration was significantly (P < 0.05) greater in the FYM-treated soil than in the metal-contaminated soils. Gram-positive counts were also 63% greater than Gram-negative counts in the FYM-treated soil. We found that effects of the relatively small heavy metal concentration caused measurable decreases in soil microbial biomass-C concentrations, acridine orange direct counts and Gram-positive counts. There were also increases in biomass specific respiration rates, and the microbial community had changed substantially, nearly 40 years after the metal inputs ceased. We conclude that, at the very least, the current EU permitted limits for heavy metals in agricultural soils should not be relaxed.