Whats under the Christmas tree? Soil acidification alters fir tree rhizosphere bacterial and eukaryotic communities, their interactions, and functional traits

Abstract

pH has been identified as a master regulator of the soil environment, controlling the solubility and availability of nutrients. As such, soil pH exerts a strong influence on indigenous microbial communities. In this study we describe a soil acidification experiment and the resulting effects on the rhizosphere communities of fir trees on a Christmas tree plantation. The acidification treatment reduced the pH of bulk soil by [~]1.4 pH units and was associated with reduced Ca, Mg, and organic matter content. Similarly, root chemistry differed due to soil acidification with roots in acidified soils showing significantly higher Al, Mn, and Zn content and reduced levels of B and Ca. 16S rRNA and 18S rRNA gene sequencing was pursued to characterize the bacterial/archaeal and eukaryotic communities in the rhizosphere soils. The acidification treatment induced dramatic and significant changes in the microbial populations, with thousands of 16S RNA gene sequence variants and hundreds of 18S rRNA gene variants being significantly different in relative abundance between the treatments. Additionally, co-occurrence networks showed that bacterial and eukaryotic interactions, network topology, and hub taxa were significantly different when constructed from the control and acidified soil rRNA gene amplicon libraries. Finally, metagenome sequencing showed that the taxonomic shifts in the community resulted in alterations to the functional traits of the dominant community members. Several biochemical pathways related to sulfur and nitrogen cycling distinguished the metagenomes generated from the control and acidified soils, demonstrating the myriad of effects soils acidification induces to rhizosphere microbes. IMPORTANCESoil pH has been identified as the property that exerts the largest influence on soil microbial populations. We employed a soil acidification experiment to investigate the effect of lowering soil pH on the bacterial and eukaryotic populations in the rhizosphere of Christmas trees. Acidification of the soils drove alterations of fir tree root chemistry and large shifts in the taxonomic and functional composition of the communities, involving pathways in sulfur and nitrogen cycling. These data demonstrate that soil pH influences are manifest across all organisms inhabiting the soil, from the host plant to the microorganisms inhabiting the rhizosphere soils. Thus, pH is an important factor that needs to be considered when investigating soil and plant health, the status of the soil microbiome, and terrestrial nutrient cycling.