The role of bacteria and mycorrhiza in plant sulfur supply

Abstract

Plant growth is highly dependent on bacteria, saprophytic, and mycorrhizal fungi which facilitate the cycling and mobilization of nutrients. Over 95% of the sulfur (S) in soil is present in an organic form. Sulfate-esters and sulfonates, the major forms of organo-S in soils, arise through deposition of biological material and are transformed through subsequent humification. Fungi and bacteria release S from sulfate-esters using sulfatases, however, release of S from sulfonates is catalyzed by a bacterial multi-component mono-oxygenase system. The asfA gene is used as a key marker in this desulfonation process to study sulfonatase activity in soil bacteria identified as Variovorax, Polaromonas, Acidovorax, and Rhodococcus. The rhizosphere is regarded as a hot spot for microbial activity and recent studies indicate that this is also the case for the mycorrhizosphere where bacteria may attach to the fungal hyphae capable of mobilizing organo-S. While current evidence is not showing sulfatase and sulfonatase activity in arbuscular mycorrhiza, their effect on the expression of plant host sulfate transporters is documented. A revision of the role of bacteria, fungi and the interactions between soil bacteria and mycorrhiza in plant S supply was conducted.

Keywords: asf gene cluster; mycorrhizal fungi; mycorrhizosphere; plant–microbe interactions; sulfatases; sulfate esters; sulfonate desulfurization.

FIGURE 1

Illustration of the sulfur cycle in soil with plant cover. Major sulfur (S) inputs to soils originate from organic litter deposition and animal droppings (blue lines). Most of this deposited S is organically bound (organo-S). Atmospheric deposition of inorganic S has greatly declined in Europe, America and elsewhere, thus is often only a minor source for plants. Organo-S (sulfate-esters and sulfonates) can be transformed by soil microbes between the two major organo-S pools or mineralized to inorganic S (green lines, thickness suggests main direction of pathway). At the same time, inorganic S can be immobilized into organo-S (green lines). While the sulfate-ester pool is largely available to both fungi and bacteria, sulfonates are primarily accessible to bacteria only and aromatic sulfonates are only available to a particular functional clade of bacteria. Bacterial sulfonate desulfurization via the mono-oxygenase multi-enzyme pathway may occur intracellular, thus polymeric sulfonate may need depolymerisation, e.g., by saprophytic fungi prior to uptake (dotted purple line). Organo-S mineralised by fungi and bacteria need to be made available for plant uptake in the form of sulfate. This may happen via sulfate uptake by mycorrhizal fungal hyphae as an intermediate step (dashed gray line). In the absence of any direct evidence of a sulfate transport system from fungus or bacterium to the plant root or symbiotic mycorrhizal hyphae, release of mineralised S through autolysis and grazing by protists and microscopic nematodes may play an import role in inorganic sulfate release and plant sulfate uptake (red lines).

FIGURE 2

Randomized axelerated maximum likelihood tree from truncated AsfA sequences obtained from aromatic sulfonate desulfurizing bacteria isolated from soil, rhizosphere, or hyphosphere alongside strains from culture collections.