Diversity and composition of soil Acidobacteria and Proteobacteria communities as a bacterial indicator of past land-use change from forest to farmland

Highlights: • High-resolution data of 16S rRNA sequencing and environmental factors were analyzed. • Land-use change from forest to farmland caused changes in pH, nutrients, anthropogenic metals, and TEAs. • Acidobacteria and Proteobacteria were most affected by land-use change. • Physicochemical variations had close associations with specific subgroups of these phyla. • These specific subgroups can be good bioindicators associated with land-use change. The land-use change from natural to managed farmland ecosystems can undergo perturbations and significantly impact soil environment and communities. To understand how anthropogenic land-use alteration determines in-depth relationships among soil environmental factors and soil bacterial communities, high-resolution characterization was performed using soil samples (27 spots × 3 depths; top 10–20 cm, middle 90–100 cm, bottom 180–190 cm) from a natural forest and a 50 year-old farmland. The soil bacterial community abundance (number of OTU's per sample) and diversity (Faith's phylogenetic diversity) was significantly higher in the top layer of farmland soil than in forest soil. However, the differences in bacterial community abundance between farmland and forest decreased with depth, suggesting that the effect of fertilization was limited to top and middle layers. The phyla Acidobacteria and Proteobacteria were distributed distinctively during the land-use change. The subgroups Gp1–3 of Acidobacteria were more abundant in the forest samples (pH 3.5–5), while Gp4–7 and Gp10 were predominant in the farmland (pH 4.5–9.5). Members belonging to α-Proteobacteria and Xanthomonadales in γ–Proteobacteria were dominant in the forest, whereas β–, δ–, and γ–Proteobacteria were relatively abundant in the farmland. Both multivariate and correlation network analyses revealed that Acidobacteria and Proteobacteria communities were significantly affected by soil pH, as well as toxic metals from pesticides (Zn, Cr, Ni, Cu, Cd, As) and terminal electron acceptors (NO₃, bioavailable Fe(III), SO₄). In line with the long history of anthropogenic fertilization, the farmland site showed high abundance of membrane and ATP-binding cassette transporter genes, suggesting the key for uptake of nutrients and for protection against toxic metals and environmental stresses. This study provides new insights into the use of both Acidobacteria and Proteobacteria community structures as a bacterial indicator for land-use change.