Effects of Bacterial Siderophore and Biofilm Synthesis on Silicate Mineral Dissolution Kinetics: Results from Experiments with Targeted Mutants

Ocean Worlds 2018 (LPI Contrib. No. 2085) 6003.pdf

EFFECTS OF BACTERIAL SIDEROPHORE AND BIOFILM SYNTHESIS ON SILICATE MINERAL DISSOLUTION KINETICS: RESULTS FROM EXPERIMENTS WITH TARGETED MUTANTS. M. D. Van Den Berghe1, A. J. West1 and K. H. Nealson1. 1Department of Earth Sciences, University of Southern California (3651 Trousdale Pkwy, Los Angeles, CA, 90089, [email protected]).

With metal ions forming the catalytic center to aeruginosa strains. Both P. aeruginosa and S. onei- countless critical biochemical reactions, it might be densis wild types also show higher growth and dis- expected that the emergence of continuous, self- solved silicon concentrations when grown in glass sustaining autocatalytic reactions that form life is flasks as opposed to Polytetrafluoroethylene flasks, linked to early interactions between mineral substrates suggesting they are facilitating active dissolution of the and sorbed organic compounds [1,2]. Biomolecule- glass flasks. mineral sorption interfaces are further suggested to These results strongly suggest that mineral phases enhance mineral dissolution and elemental release [3]. can act as a substrate supporting bacterial growth, and Notably, many microorganisms synthesize sidero- that siderophores can act as an effective mechanism for phores, organic compounds with extremely high iron- bacteria to dissolve and acquire micronutrients directly binding affinities, in order to isolate iron and improve from mineral, and even glass, phases. Thick, multi- its acquisition. However much remains unknown about layered, redox-active biofilms can also have abrasive siderophores’ role in the release of iron contained in qualities that can lead to mineral dissolution and nutri- silicate minerals, and thus their impact on dissolution ent release, supporting microbial growth even in the kinetics [4]. Many bacteria also form thick, redox- absence of siderophores. The precise mechanisms in- active biofilms on mineral surfaces in order to create volved in biofilm-driven mineral dissolution may in- micro-environments favorable for growth, which role is clude extra-cellular electron shuttles such as phena- also unclear with respect to silicate mineral dissolution zines, and secondary metabolites such as lactate, py- [5]. These combined effects however suggest active ruvate, malonate or ketogluconic acid, all products of mechanisms of nutrient acquisition directly from min- glucose metabolism and fermentation [5], known to act eral phases, processes so far largely overlooked and as effective surface sorbents [6]. Such metabolites may poorly understood. Constraining siderophore and bio- be found in very high concentrations in biofilms and film influences on mineral phases therefore has the may further contribute to mineral dissolution. These potential to answer long standing questions about the experiments thus point to the potentially high im- biological controls on silicate weathering, the metabol- portance of biofilms as possible hot-spots of mineral ic potential driving bacteria-mineral interactions, as dissolution. Our ongoing research will further charac- well as the limits of life in ocean and sub-surface envi- terize and quantify these processes through advanced ronments, and the coevolution of life and Earth. metabolomics and imaging experiments, as well as Our current research is aiming to characterize and identify them in the natural, limiting environment of quantify the effects of bacterial siderophore and bio- oceanic crustal fluids. film synthesis on the dissolution kinetics of silicate References: minerals. We have adopted a new approach to this 1 Belmonte, L. and Mansy, S.S. (2016) Elements 12, problem, using targeted gene deletion mutants on envi- 413–418 ronmentally relevant bacteria (S. oneidensis and P. 2 Hazen, R.M. and Sverjensky, D.A. (2010) Cold aeruginosa) in order isolate specific metabolic effects Spring Harb. Perspect. Biol. 2, a002162–a002162 on bacteria-mineral interactions. Batch experiments 3 Kraemer, S.M. (2005) Rev. Mineral. Geochem. 59, with S. oneidensis wild type (MR-1) and a siderophore 53–84 synthesis gene deletion mutant strain, both grown in 4 Dhungana, S. and Crumbliss, A.L. (2005) Geomi- iron-deplete minimal media amended with olivine as crobiol. J. 22, 87–98 sole source of iron, show a pronounced growth penalty 5 Glasser, N.R. et al. (2014) Mol. Microbiol. 92, for the siderophore deletion mutant. P. aeruginosa can 399–412 however synthesize centimeter-thick, multi-layered 6 Stumm, W. (1995) Aquatic Chemistry 244 (Huang, redox-active biofilms, and preliminary experiments C. P. et al., eds), pp. 1–32, American Chemical So- with wild type (PA-14) and a siderophore synthesis ciety. gene deletion mutants, also grown in iron-deplete min-

imal media amended with olivine, show no growth penalty for the gene deletion mutant. Dissolved silicon concentrations, measured as a proxy for olivine dissolution, also increased in growth experiments for both P.