Potential use of pineapple (ananas comosus L.) and cadmium tolerant bacteria to reduce cadmium toxicity in soil

Abstract

Cadmium (Cd) is a toxic metal that occurs in the environment naturally and as a pollutant from industrial and agricultural sources. The Cd concentration of agricultural soils in Thailand has increased during the last few decades as a consequence of mining activities. This toxic metal is allocated to edible plant parts and moves into the food chain via rice grains in some provinces in the Northern part of Thailand. Pineapple (Ananas comosus L.) is the most widely cultivated tropical fruit in Thailand and possesses the photosynthetic specialisation of crassulacean acid metabolism (CAM). Since CAM plants are generally tolerant to abiotic stress, it was hypothesised that pineapple would be relatively tolerant to Cd and could potentially be grown as a crop in Cd-contaminated soils. The present study determined the effect of Cd on photosynthetic performance, growth and Cd accumulation in different parts of pineapple. Pineapple plants grown in Cd-contaminated soil did not show any visual symptoms of toxicity and whilst light use efficiency (Fv/Fm) and rates of net dark CO2 uptake were reduced by Cd treatment, biomass reductions were only 14% of control at the highest concentration of Cd (150 mg Cd kg-1). Levels of Cd accumulated by pineapple increased as the Cd concentration in soil increased. Pineapple plants took up Cd from the soil, resulting in lower Cd concentrations in the rhizosphere soil compared with the bulk soil. The soil-extractable Cd decreased over time which may have been due to the uptake of Cd by plant and to remaining metal ions becoming more tightly bound with organic materials or root exudates. Calculated as Cd μg per g dry weight, roots accumulated higher amount of Cd than shoots. Short-term and long-term exposure to Cd resulted in a reduction in the numbers and diversity of soil microbes as indicated using plate count and DGGE techniques. The pineapple rhizosphere exhibited increased numbers of bacteria and fungi and a distinct and more diverse bacterial population when compared to bulk soil. Cd pollution of soil reduced both microbial numbers and bacterial diversity of all soil samples. Certain bacteria in the phyla Nitrospirae, Verrucomicrobia, Acidobacteria and Chloroflexi were only present in Cd-contaminated soil. Cd-resistant bacteria were isolated from the rhizosphere of pineapple grown in Cd-contaminated soil and were subsequently used as inoculants in an effort to improve plant growth and reduce Cd toxicity. Nine isolates of Cd-resistant bacteria were isolated from the rhizosphere soil of pineapple. Two bacterial strains, Bacillus firmus and Arthrobacter humicola were identified as having the potential to alleviate Cd toxicity in soil since both isolates were found to accumulate Cd at 17.21 and 19.83 mg Cd per g biomass at an initial Cd level of 50 mg Cd l-1. Application of B. firmus and A. humicola near the root zone of pineapple grown in Cd-contaminated soil resulted in an increased uptake of nutrients compared with non-inoculated plants. In addition, soil inoculation resulted in higher rates of dark CO2 uptake, reduced Cd accumulation and increased biomass of pineapple plants grown in Cd-contaminated soil as compared with non-inoculated plants. Overall it would appear that pineapple could be grown commercially in Cd contaminated soils as it is relatively Cd resistant and it would also reduce total and extractable Cd soil levels over time. Bacterial inoculation of soil could be used to improve pineapple growth but the financial viability of this would need to be determined.