From soil to symbiosis: elemental filtering in a termite-fungus mutualism

All organisms require a balanced supply of over 20 chemical elements, and even small imbalances can limit performance and fitness. Organisms thus employ diverse adaptations for acquiring and regulating balanced combinations of these elemental resources. In farming mutualisms, adaptations of domesticated crops can guide the accumulation of critical elements from soil or mulched detritus for partner use. It is therefore reasonable to predict systematic shifts in elemental abundance and variance across farming stages – from substrate provisioning and crop assimilation to the final production of edible yield. We tested this hypothesis with fungus-farming termites that cultivate fungi in combs built from a mix of termite-provisioned organic matter and soil, in exchange for edible nutrient-rich fungal nodule structures. Using Inductively Coupled Plasma Mass Spectrometry (ICP-MS), we quantified 24 elements across fungus-farming stages – from soils, through termite guts and fresh and mature fungal combs, to final nodules. Our findings suggest 1) that termite foraging represents an initial nutritional filtering stage that enriches biogenic elemental building blocks for macronutrients (K, S, Na, and Ca) while reducing several non-biogenic and potentially toxic elements (As and Pb) and 2) fungal nodules constitute a final nutritional filtering stage that concentrates a suite of biogenic elements (P, K, S, Cu, and Zn) alongside accumulation of certain non-biogenic elements (Cd, and Tl). Within fungus gardens, elemental compositions are homogenised in freshly-build combs relative to the mulch deposited from termite guts. These patterns suggest elemental filtering as reciprocal provisioning between farmers and crops, offering a framework to understand how complex mutualistic nutritional systems regulate and ultimately affect element cycling in soil ecosystems. • Fungus farming involves systematic elemental shifts across farming stages • Termite provisioning involves enriching key elements compared to soils • Edible fungal structures make essential elements available to termite farmers • Potentially harmful elements (e.g. Pb, Ba and As) diminish at distinct farming stages • Provisioning strategies offer insights into elemental fluxes in nutritional symbioses