Reviews and syntheses: Biological weathering and its consequences at different spatial levels – from nanoscale to global scale

Abstract

Plant nutrients can be recycled through microbial decomposition of organic matter but replacement of base cations and phosphorus, lost through harvesting of biomass/biofuels or leaching, requires de novo supply of fresh nutrients released through weathering of soil parent material (minerals and rocks). Weathering involves physical and chemical processes that are modified by biological activity of plants, microorganisms and animals. This article reviews recent progress made in understanding biological processes contributing to weathering. A perspective of increasing spatial scale is adopted, examining the consequences of biological activity for weathering from nanoscale interactions, through in vitro and in planta microcosm and mesocosm studies, to field experiments, and finally ecosystem and global level effects. The topics discussed include the physical alteration of minerals and mineral surfaces; the composition, amounts, chemical properties, and effects of plant and microbial secretions; and the role of carbon flow (including stabilisation and sequestration of C in organic and inorganic forms). Although the predominant focus is on the effects of fungi in forest ecosystems, the properties of biofilms, including bacterial interactions, are also discussed. The implications of these biological processes for modelling are discussed, and we attempt to identify some key questions and knowledge gaps, as well as experimental approaches and areas of research in which future studies are likely to yield useful results. A particular focus of this article is to improve the representation of the ways in which biological processes complement physical and chemical processes that mobilise mineral elements, making them available for plant uptake. This is necessary to produce better estimates of weathering that are required for sustainable management of forests in a post-fossil-fuel economy. While there are abundant examples of nanometre- and micrometre-scale physical interactions between microorganisms and different minerals, opinion appears to be divided with respect to the quantitative significance of these observations for overall weathering. Numerous in vitro experiments and microcosm studies involving plants and their associated microorganisms suggest that the allocation of plant-derived carbon, mineral dissolution and plant nutrient status are tightly coupled, but there is still disagreement about the extent to which these processes contribute to field-scale observations. Apart from providing dynamically responsive pathways for the allocation of plant-derived carbon to power dissolution of minerals, mycorrhizal mycelia provide conduits for the long-distance transportation of weathering products back to plants that are also quantitatively significant sinks for released nutrients. These mycelial pathways bridge heterogeneous substrates, reducing the influence of local variation in C:N ratios. The production of polysaccharide matrices by biofilms of interacting bacteria and/or fungi at interfaces with mineral surfaces and roots influences patterns of production of antibiotics and quorum sensing molecules, with concomitant effects on microbial community structure, and the qualitative and quantitative composition of mineral-solubilising compounds and weathering products. Patterns of carbon allocation and nutrient mobilisation from both organic and inorganic substrates have been studied at larger spatial and temporal scales, including both ecosystem and global levels, and there is a generally wider degree of acceptance of the “systemic” effects of microorganisms on patterns of nutrient mobilisation. Theories about the evolutionary development of weathering processes have been advanced but there is still a lack of information connecting processes at different spatial scales. Detailed studies of the liquid chemistry of local weathering sites at the micrometre scale, together with upscaling to soil-scale dissolution rates, are advocated, as well as new approaches involving stable isotopes.