Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate

Abstract

The osmoadaptation of most micro-organisms involves the accumulation of K(+) ions and one or more of a restricted range of low molecular mass organic solutes, collectively termed 'compatible solutes'. These solutes are accumulated to high intracellular concentrations, in order to balance the osmotic pressure of the growth medium and maintain cell turgor pressure, which provides the driving force for cell extension growth. In this review, I discuss the alternative roles which compatible solutes may also play as intracellular reserves of carbon, energy and nitrogen, and as more general stress metabolites involved in protection of cells against other environmental stresses including heat, desiccation and freezing. Thus, the evolutionary selection for the accumulation of a specific compatible solute may not depend solely upon its function during osmoadaptation, but also upon the secondary benefits its accumulation provides, such as increased tolerance of other environmental stresses prevalent in the organism's niche or even anti-herbivory or dispersal functions in the case of dimethylsulfoniopropionate (DMSP). In the second part of the review, I discuss the ecological consequences of the release of compatible solutes to the environment, where they can provide sources of compatible solutes, carbon, nitrogen and energy for other members of the micro-flora. Finally, at the global scale the metabolism of specific compatible solutes (betaines and DMSP) in brackish water, marine and hypersaline environments may influence global climate, due to the production of the trace gases, methane and dimethylsulfide (DMS) and in the case of DMS, also couple the marine and terrestrial sulfur cycles.

Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa

“…The coexistence of choline import, choline oxidation to GB, and predicted regulated export of GB suggests that acquisition of abundant choline by one cell population may result in efflux of GB capable of providing osmoprotectants to other cells within the community, as described in work with Vibrio cholerae and other Vibrio species (101) and discussed by Welsh (102). In a mechanistic examination of this phenomenon, Hoffmann and colleagues recently reported the sharing and recycling of proline between cells of Bacillus subtilis, providing direct evidence of osmoprotectants as a piece of microbial communal property (103).…”

“…Therefore, perhaps GB is stored in these bacteria to provide enhanced survival and recovery from unexpected insults that provide a survival benefit versus bacteria that do not have such storage systems. A second possibility is that choline and GB represent relatively innocuous means of storing a high-N/C-ratio compound to provide a readily utilizable nitrogen source (102). For this role, it is important that catabolism of choline and GB is not under catabolite repression control during nitrogen starvation (86).…”

“…Here, I present three potential roles for these choline and GB pools that are not mutually exclusive. First, these bacteria may maintain these pools as preemptive hedges against future insults (102). GB is a protectant against osmostress, temperature stress, and oxidative stress, and has a role in maintenance of intracellular pH (98,(108)(109)(110).…”

Dimethylsulfoniopropionate in corals and its interrelations with bacterial assemblages in coral surface mucus

“…[21] The relative incidence of these competing microbial pathways has important consequences for the marine sulfur cycle and for DMS release into the atmosphere. [2,22] Besides its role as a carbon and sulfur source for bacteria, DMSP has been shown to be involved in osmoprotection in algae and bacteria, [6,23] to be a precursor of cues for chemosensory attraction for a variety of organisms from bacteria to vertebrates [24,25] and to be an antiviral defence mechanism. [26] Most importantly, DMSP and its enzymatic breakdown products, DMS, acrylate, dimethylsulfoxide (DMSO) and methane sulfinic acid (MSNA), are scavengers of hydroxyl radicals and other reactive oxygen species (ROS) in marine algae.…”

Bacterial flavin-containing monooxygenase is trimethylamine monooxygenase

“…In the marine environment, methylated amines are released as a result of degradation of quaternary amine osmoregulators, such as glycine betaine, which are used by marine organisms to counteract water stress (19)(20)(21). Once released into the environment, methylated amines can be used by microorganisms as a C or N source.…”