Microbiology of sugar‐rich environments: diversity, ecology and system constraints

Abstract

Microbial habitats that contain an excess of carbohydrate in the form of sugar are widespread in the microbial biosphere. Depending on the type of sugar, prevailing water activity and other substances present, sugar-rich environments can be highly dynamic or relatively stable, osmotically stressful, and/or destabilizing for macromolecular systems, and can thereby strongly impact the microbial ecology. Here, we review the microbiology of different high-sugar habitats, including their microbial diversity and physicochemical parameters, which act to impact microbial community assembly and constrain the ecosystem. Saturated sugar beet juice and floral nectar are used as case studies to explore the differences between the microbial ecologies of low and higher water-activity habitats respectively. Nectar is a paradigm of an open, dynamic and biodiverse habitat populated by many microbial taxa, often yeasts and bacteria such as, amongst many others, Metschnikowia spp. and Acinetobacter spp., respectively. By contrast, thick juice is a relatively stable, species-poor habitat and is typically dominated by a single, xerotolerant bacterium (Tetragenococcus halophilus). A number of high-sugar habitats contain chaotropic solutes (e.g. ethyl acetate, phenols, ethanol, fructose and glycerol) and hydrophobic stressors (e.g. ethyl octanoate, hexane, octanol and isoamyl acetate), all of which can induce chaotropicity-mediated stresses that inhibit or prevent multiplication of microbes. Additionally, temperature, pH, nutrition, microbial dispersion and habitat history can determine or constrain the microbiology of high-sugar milieux. Findings are discussed in relation to a number of unanswered scientific questions.

Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms

“…S. cerevisiae and Z. mobilis) [29 ], gastrointestinal tracts, diverse anoxic sediments, and the production waters surrounding oil deposits (e.g. Clostridium spp.…”

Non-nodular Endophytic Bacterial Symbiosis and the Nitrogen Fixation of Gluconacetobacter diazotrophicus

“…Interestingly, however, this gene is considered only a secondary low affinity potassium transporter for bacteria generally and certainly has not been implicated in the regulation of osmotic stress [35]. Hence, this high-affinity potassium transport role of the KupA protein by which G. diazotrophicus regulates osmotic stress in high sucrose concentrations, is different from other bacterial species [27]. G. diazotrophicus seems to have a larger number of isoforms of enzymatic systems involved in osmotolerance [30].…”

“…The presence of solutes such as, salts or sugars can create an osmotically stressful environment for bacteria and relatively few species have mechanisms that allow cell multiplication under extreme conditions of <0.70 aw [26,27]. Plant sap generally has water activity values between 0.99 and 0.96 aw (and pH 4.4-8.0); levels that are able to support a phylogenetically diverse groups of micro-organisms, including plant pathogens, plant and insect bacterial and fungal endosymbionts [27].…”

“…Osmotic pressure is regulated in many bacteria by the movement of potassium ions in to and out of the cell [34]. In G. diazotrophicus sucrose tolerance is, at least partially, achieved through genes encoding for the KupA protein [27]. Interestingly, however, this gene is considered only a secondary low affinity potassium transporter for bacteria generally and certainly has not been implicated in the regulation of osmotic stress [35].…”

“…In addition to the sap of the host plant other sites of high sucrose include floral nectar, plant fruits and fruit juices as well as the guts of sugar-feeding insects and the rhizosphere [27]. Studies of bacterial-insect symbiosis have demonstrated that the AAB are capable of establishing symbiotic relationships with insects that rely on a sugar-based diet [36].…”