Can transgenic maize affect soil microbial communities?

Abstract

The aim of the experiment was to determine if temporal variations of belowground activity reflect the influence of the Cry1Ab protein from transgenic maize on soil bacteria and, hence, on a regulatory change of the microbial community (ability to metabolize sources belonging to different chemical guilds) and/or a change in numerical abundance of their cells. Litter placement is known for its strong influence on the soil decomposer communities. The effects of the addition of crop residues on respiration and catabolic activities of the bacterial community were examined in microcosm experiments. Four cultivars of Zea mays L. of two different isolines (each one including the conventional crop and its Bacillus thuringiensis cultivar) and one control of bulk soil were included in the experimental design. The growth models suggest a dichotomy between soils amended with either conventional or transgenic maize residues. The Cry1Ab protein appeared to influence the composition of the microbial community. The highly enhanced soil respiration observed during the first 72 h after the addition of Bt-maize residues can be interpreted as being related to the presence of the transgenic crop residues. This result was confirmed by agar plate counting, as the averages of the colony-forming units of soils in conventional treatments were about one-third of those treated with transgenic straw. Furthermore, the addition of Bt-maize appeared to induce increased microbial consumption of carbohydrates in BIOLOG EcoPlates. Three weeks after the addition of maize residues to the soils, no differences between the consumption rate of specific chemical guilds by bacteria in soils amended with transgenic maize and bacteria in soils amended with conventional maize were detectable. Reaped crop residues, comparable to post-harvest maize straw (a common practice in current agriculture), rapidly influence the soil bacterial cells at a functional level. Overall, these data support the existence of short Bt-induced ecological shifts in the microbial communities of croplands' soils.

Figure 1. Bt Parasporal Crystals in Maize and One Amended Soil

(A) Photo of B. thuringiensis (ssp. kurstaki) with protein crystals, hyaline spores, and vegetative cells (elongate, opaque cells) by courtesy of Dr. Bjarne Munk Hansen, Danmarks Miljøundersøgelser. (B) Transgenic crop residues and soil sample after the addition of reaped maize straw shortly before starting the experiment (complete straw analysis available as Table S1).

Figure 2. Amount of CO₂-C after Addition of Maize Residues

Temporal variance in gross soil respiration of a stagnic luvisol after the addition of maize straw. Dotted lines for crop residues from conventional maize, continuous lines for transgenic maize. Untreated soils without any addition of straw showed initial respiration values of 12 μg CO₂-C at d 0 (n = 5). MON810 (Novelis) and Event 176 (Valmont) are transgenic. The differences between these cultivars and their mother plants were significant: conventional straw did not enhance soil respiration as much as transgenic straw (ANOVA: p < 0.00001).

Figure 3. Plate Counts in Time

CFU growing curves in amended soils. Dotted lines for crop residues from conventional maize, continuous lines for transgenic maize. Transgenic maize straws show a much higher number of CFUs than conventional straws during the first week (ANOVA: p = 0.0296), but the differences between all four maize cultivars are not significant (ANOVA: p = 0.1389).

Figure 4. Multivariate Analysis of the Soils Amended with Transgenic Maize

PRCs of the summarized metabolic fingerprints of the two Bt-maize straws (both Nobilis and Prelude as conventional isoline control level as horizontal x-axis) according to all BIOLOG EcoPlate carbon sources (n = 3 in duplicate). Day 3 is the most significant by time for all maize cultivars (SD = ± 0.242, p = 0.064, F-ratio = 2.66).

Figure 5. Examples of Amended Soils at the Beginning of the Experiment

Some soil samples before entering the 1.0-L pots after the addition of crop residues (reaped maize straw, see Figure 1B). Please note the slightly different colors.