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Life at Low Water Activity

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Life at Low Water Activity Published online 12 July 2004 Life at low water activity W. D. Grant Department of Infection, Immunity and Inflammation, University of Leicester, Maurice Shock Building, University Road, Leicester LE1 9HN, UK ([email protected]) Two major types of environment provide habitats for the most xerophilic organisms known: foods pre- served by some form of dehydration or enhanced sugar levels, and hypersaline sites where water availability is limited by a high concentration of salts (usually NaCl). These environments are essentially microbial habitats, with high-sugar foods being dominated by xerophilic (sometimes called osmophilic) filamentous fungi and yeasts, some of which are capable of growth at a water activity (aw) of 0.61, the lowest aw value for growth recorded to date. By contrast, high-salt environments are almost exclusively populated by prokaryotes, notably the haloarchaea, capable of growing in saturated NaCl (aw 0.75). Different strategies are employed for combating the osmotic stress imposed by high levels of solutes in the environment. Eukaryotes and most prokaryotes synthesize or accumulate organic so-called ‘compatible solutes’ (osmolytes) that have counterbalancing osmotic potential. A restricted range of bacteria and the haloar- chaea counterbalance osmotic stress imposed by NaCl by accumulating equivalent amounts of KCl. Haloarchaea become entrapped and survive for long periods inside halite (NaCl) crystals. They are also found in ancient subterranean halite (NaCl) deposits, leading to speculation about survival over geological time periods. Keywords: xerophiles; halophiles; haloarchaea; hypersaline lakes; osmoadaptation; microbial longevity 1. INTRODUCTION aw = P/P0 = n1/n1 ϩ n2, There are two major types of environment in which water where n is moles of solvent (water); n is moles of solute; availability can become limiting for an organism. One is 1 2 P is vapour pressure of solution and P is vapour pressure a solution in which water availability is determined by the 0 of pure water at the same temperature. concentration of solutes in that solution, whereas in the Water activity is simply the effective water content other case, the availability is determined mainly by capil- expressed as its mole fraction, which is also reflected in lary and surface-binding effects, as, for example, in a com- the relative humidity that is reached at equilibrium in a plex physically heterogeneous environment such as soil. sealed container where a hygroscopic product or solution There is no a priori reason to suppose that an organism has been placed. would react differently to water stress imposed by either It follows that pure water has a water activity of 1 and set of conditions, but in practice, in the heterogeneous all other solutions have values of a less than 1. The environment there are other surface-associated effects that w advantages of using a include its ready application to sol- complicate and compromise any quantitative analysis. For w utions and the ease with which it can be measured. It is that reason, the vast majority of laboratory studies relate less useful in complex particulate systems like soil, where to environments where water availability is imposed by the a different term ␺ is often used, which addresses the ques- presence of solutes. A widely adopted way of defining the tion of capillarity. However, capillarity is negligible for availability of water in a particular environment is the use organisms in essentially liquid environments and can be of the term a (water activity), originally developed by the w ignored under these conditions. The underlying theory of food and pharmaceutical industry, where it is used to ␺ and the consideration of the capillary component for determine shelf life and quality of product. The simple environments such as soil is described in Griffin (1981) water content of a material (percentage water) takes no and Griffin & Luard (1979) and is not considered further account of water that is thermodynamically available and in this review, which is largely concerned with homo- has little application to the majority of situations. Water geneous liquid environments. activity (a ) is based on Raoult’s Law for ideal solutions w Organisms capable of growing under conditions of low and does not take into consideration solute interactions water activity are commonly referred to under the blanket with components other than water; accordingly the accu- terms xerotolerant or xerophilic (although see later in this racy of the calculation is greater for dilute solutions. Put section). The suffix ‘tolerant’ indicates that the organism simply: is capable of growth conditions of low aw, but does not necessarily require low aw for growth. The suffix ‘philic’ on the other hand indicates that the organisms actually One contribution of 16 to a Discussion Meeting Issue ‘The molecular require low aw conditions for growth. Generally, xerophilic basis of life: is life possible without water?’. organisms are capable of growing at aw values lower than Phil. Trans. R. Soc. Lond. B (2004) 359, 1249–1267 1249 2004 The Royal Society DOI 10.1098/rstb.2004.1502 1250 W. D. Grant Life at low water activity xerotolerant organisms, but there are exceptions to this geology of the area where they develop, for example by general rule, particularly among the prokaryotes, where the resolution of salt deposits from a previous evaporative there are organisms in both categories capable of growing event, or significant leaching of ions from the surrounding in saturated salt (Vreeland 1987; Brown 1990). Two geology. The Dead Sea is an example of a hypersaline major types of environment provide habitats for the most environment profoundly influenced by an earlier Mg2ϩ- xerophilic organisms, namely foods preserved by some rich brine, somewhat depleted in Naϩ. Eugster & Hardie form of dehydration or organic solute-promoted lowering (1978) have attempted to define the key geological and of aw, and saline lakes, where low aw values are a conse- chemical features that influence how a hypersaline brine quence of inorganic ions. These environments are essen- develops. tially exclusively populated by micro-organisms and Apart from total salinity and ionic composition, pH is contain the most xerophilic organisms described to date. important in determining the composition of any Saline soils, often adjacent to saline lakes, share micro- microbial population in any hypersaline brine. The organisms in common with saline lakes (Ventosa et al. amount of Ca2ϩ (and to a lesser extent Mg2ϩ) is critical 1998a). in determining the final pH of a brine. The equilibrium 2Ϫ Ϫ The stresses imposed by ions and organic solutes are between CO3 , HCO3 and CO2 is one of the principal not necessarily the same. Many xerophilic micro- buffer systems in the aquatic environment, being, for organisms from high-sugar foods are tolerant of low aw example, one of the buffer systems that maintains the pH levels imposed by ions. Zygogaccharomyces rouxii, a xero- of seawater. The presence of Ca2ϩ, which removes alka- 2Ϫ philic yeast food-spoilage organism, will grow in media line CO3 through the precipitation of insoluble calcite containing 20% (w/v) NaCl (Eriksen & McKenna 1999) (CaCO3), obviously influences this equilibrium. Brines and in media supplemented with glucose or glycerol at derived from seawater have relatively high concentrations 2ϩ similar aw levels (although it will grow at much lower aw of Ca and remain around neutrality even after extensive 2ϩ levels in these media). The limiting aw for food-poisoning concentration because the molarity of Ca always 2Ϫ strains of Staphylococcus aureus isolated from food is the exceeds that of CO3 . Profoundly alkaline lakes develop same whether the solute is salt or sugars (Scott 1957). in areas where the surrounding geology is deficient in However, the converse is generally not true—micro- Ca2ϩ, for example in the East African Rift Valley. Here, ϩ organisms growing in saturated salt lakes (aw 0.75) for surrounding high Na trachyte lavas are deficient in both 2ϩ 2ϩ example, as a rule, cannot grow in media of similar aw Ca and Mg , allowing the development of lakes with solely imposed by organic solutes (Kushner 1978). In pH values in excess of 11 (Grant & Tindall 1986; Grant 2ϩ particular, micro-organisms inhabiting low aw, high-salt et al. 1990; Jones et al. 1998). Levels of Mg also influ- 2Ϫ environments have features specifically adapted to higher ence the systems by removing CO3 as dolomite levels of ions, in addition to an overarching adaptation to (CaMg(CO3)2), and in the case of the Dead Sea, whose low aw values. Such organisms are generally described as composition is markedly influenced by a previous Mg-rich halophilic or halotolerant rather than xerophilic or xerotol- evaporite, cause slightly acidic conditions through the gen- erant. Hence, the terms xerophilic and xerotolerant are eration of Mg2ϩ minerals such as sepiolite, which gener- often now restricted to describing those organisms grow- ates Hϩ during the precipitative process. Figure 1 shows ing at aw values imposed by other than inorganic ions, and a schematic representation of the genesis of major neutral this usage is followed here. There are a number of subcat- and alkaline hypersaline lake types. High levels of other egories of terms for organisms that have intermediate ions in the surrounding topography will also influence the properties of halotolerance and halophily, not all of which final composition, and there are exceptional hypersaline are taken to mean the same thing by different authors (see lakes dominated by Ca2ϩ. Javor (1989) should be con- Grant et al. 1998a). This review is concerned with organ- sulted for a list of brine types and the chemical and physi- isms, the majority of which are capable of growth at aw cal parameters that influence their development. values of 0.80 or less, whether they be xerophilic/halophilic Surface hypersaline lakes and solar salterns are the or xerotolerant/halotolerant.
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