Cycling of Biogenic Mn-Oxides in a Model Microbial Predator-Prey System

Abstract

The phase distribution and bioavailability of both essential and toxic trace metals can be profoundly impacted by trophic transfer in microbial food webs. A model microbial predator-prey system was used to elucidate the possible transformations of biogenic manganese oxides as they were consumed by protozoan predators along with their bacterial prey. The ciliated protozoan Tetrahymena thermophila and the Mn-oxidizing bacterium Leptothrix discophora SS-1 were chosen as predator and prey species, respectively. The following processes were evaluated: adsorption and pinocytosis of Mn(II), regeneration and bioaccumulation of biogenic Mn-oxides, and excretion of Mn associated with waste matter. Changes in Mn oxidation state and phase distribution were assessed by observation of dissolved Mn(II) concentrations coupled with a comparison of Mn-oxide and total Mn concentration over time. Mn(II) adsorption to and pinocytosis by T. thermophila were not significant at Mn levels up to 100 μM. At the experimental pH of 7.0, the oxidation state and phase distribution of Mn at Mn levels up to 60 μM was not affected by T. thermophila's predation of L. discophora strain SS-1 and the accompanying consumption of Mn-oxide particles. Addition of an Mn+2 spike to one reactor revealed that ingested biogenic Mn(III/IV)-oxide solubilized as dissolved Mn(II) would have been quickly re-oxidized or adsorbed under the experimental conditions. Although biogenic Mn-oxide particles were observed by microscope to be consumed by T. thermophila during grazing, this consumption is likely to have represented only a small portion of the total Mn in the system. The overall results obtained suggest that the consumption of biogenic Mn-oxide particles associated with bacterial prey by microbial predators does not significantly change the solid/solution phase distribution of Mn and it does not have a major impact on the geochemical cycling of Mn. An adaptive advantage postulated as a rationale for bacterial catalysis of Mn(II) oxidation is that the resulting extracellular coating of biogenic Mn-oxide may protect cells from microbial predators. The observed reduction in L. discophora population size through predation by T. thermophila was comparable at all levels of biogenic Mn oxide tested and no beneficial effect could be observed.