Organic Stabilization of Extracellular Elemental Sulfur in a Sulfurovum-Rich Biofilm: A New Role for Extracellular Polymeric Substances?

Brandi Cron,Jennifer L Macalady,Julie Cosmidis

doi:10.3389/fmicb.2021.720101

Abstract

This work shines light on the role of extracellular polymeric substance (EPS) in the formation and preservation of elemental sulfur biominerals produced by sulfur-oxidizing bacteria. We characterized elemental sulfur particles produced within a Sulfurovum-rich biofilm in the Frasassi Cave System (Italy). The particles adopt spherical and bipyramidal morphologies, and display both stable (α-S8) and metastable (β-S8) crystal structures. Elemental sulfur is embedded within a dense matrix of EPS, and the particles are surrounded by organic envelopes rich in amide and carboxylic groups. Organic encapsulation and the presence of metastable crystal structures are consistent with elemental sulfur organomineralization, i.e., the formation and stabilization of elemental sulfur in the presence of organics, a mechanism that has previously been observed in laboratory studies. This research provides new evidence for the important role of microbial EPS in mineral formation in the environment. We hypothesize that the extracellular organics are used by sulfur-oxidizing bacteria for the stabilization of elemental sulfur minerals outside of the cell wall as a store of chemical energy. The stabilization of energy sources (in the form of a solid electron acceptor) in biofilms is a potential new role for microbial EPS that requires further investigation.

Highlights

Elemental sulfur [S(0)] is an intermediate of the biogeochemical sulfur cycle found in many natural environments, such as marine sediments, marine and lacustrine water columns, cold or hot springs, hydrothermal environments, salt marshes, and caves (Zerkle et al, 2010; Findlay et al, 2014; Hamilton et al, 2015; Lau et al, 2017; Jørgensen et al, 2019)
Scanning electron microscopy imaging combined with Energy-dispersive X-ray spectroscopy (EDXS) analyses of the Sulfurovum-dominated biofilms revealed abundant sulfur-rich particles within a dense matrix of extracellular polymeric substance (EPS) (Figure 2; Supplementary Figures S1, S2)
The particles appear as spheroids and bipyramidal crystals, which are sometimes fused into elongated chains (Figure 2A; Supplementary Figure S1)

Summary

Introduction

Elemental sulfur [S(0)] is an intermediate of the biogeochemical sulfur cycle found in many natural environments, such as marine sediments, marine and lacustrine water columns, cold or hot springs, hydrothermal environments, salt marshes, and caves (Zerkle et al, 2010; Findlay et al, 2014; Hamilton et al, 2015; Lau et al, 2017; Jørgensen et al, 2019). A wide diversity of microorganisms can oxidize sulfide, polysulfides, or thiosulfate and precipitate S(0) through both phototrophic and chemotrophic pathways (Kleinjan et al, 2003; Dahl and Prange, 2006). Elemental Sulfur Stabilization in Biofilms formed S(0) can be used as a source of energy for a wide diversity of S-oxidizers, S-reducers, and microorganisms that perform S(0) disproportionation (Warthmann et al, 1992; Dahl, 2020a). Biogenic S(0) is deposited either intracellularly or extracellularly (Kleinjan et al, 2003; Dahl and Prange, 2006; Maki, 2013). Most studies on microbial S(0) biomineralization so far have focused on microorganisms forming intracellular S(0) globules, for instance Allochromatium vinosum, Acidithiobacillus ferrooxidans, Thiothrix spp., or large colorless SOB, such as Thiomargarita namibiensis, Thioploca spp., or Beggiatoa spp. More work is needed to decipher the formation mechanisms of extracellular S(0) and to characterize its properties

Methods

Results

Conclusion