Evidence for a temperature acclimation mechanism in bacteria: an empirical test of a membrane‐mediated trade‐off

Abstract

Summary1. Shifts in bacterial community composition along temporal and spatial temperature gradients occur in a wide range of habitats and have potentially important implications for ecosystem functioning. However, it is often challenging to empirically link an adaptation or acclimation that defines environmental niche or biogeography with a quantifiable phenotype, especially in micro-organisms. 2. Here we evaluate a possible mechanistic explanation for shifts in bacterioplankton community composition in response to temperature by testing a previously hypothesized membrane mediated trade-off between resource acquisition and respiratory costs. 3. We isolated two strains of Flavobacterium sp. at two temperatures (cold isolate and warm isolate) from the epilimnion of a small temperate lake in North Central Minnesota. 4. Compared with the cold isolate the warm isolate had higher growth rate, higher carrying capacity, lower lag time and lower respiration at the high temperature and lower phosphorus uptake at the low temperature. We also observed significant differences in membrane lipid composition between isolates and between environments that were consistent with adjustments necessary to maintain membrane fluidity at different temperatures. 5. Our results suggest that temperature acclimation in planktonic bacteria is, in part, a resource-dependent membrane-facilitated phenomenon. This study provides an explicit example of how a quantifiable phenotype can be linked through physiology to competitive ability and environmental niche.

The under‐ice microbiome of seasonally frozen lakes

“…A fourth example for high bacterial abundance and biomass under the ice of a temperate, deep, and oligotrophic lake (Lake Stechlin) is provided below. These examples clearly demonstrate that bacteria are not necessarily limited by low temperatures and inorganic nutrient availability during winter and, instead, seem to be limited by low availability of organic carbon substrates due to limited phytoplankton growth (Hall et al 2010). …”

“…For example, some phytoplankton taxa that form resting spores only occur in temperate or boreal areas where lakes freeze in winter (Hargraves and French 1983). Spore formation is triggered by decreasing temperatures and light, with germination upon increasing light levels (Hargraves and French 1983;McQuoid and Hobson 1996).…”

“…Microbial membranes are more fluid at high temperatures so that nutrient uptake is more efficient, but the fitness cost to this fluidity is increased respiration. At cold temperatures, microbial membranes are more rigid, which restricts nutrient uptake but increases respiration efficiency (Hall et al 2010). Though some microbial taxa may be more cold-or warm-adapted, the ability of some community members to change their membrane fluidity (by replacing lipids) may be one way to control metabolism during transitional periods at ice-on and ice-off.…”

“…This can be achieved in various ways. For example, some bacteria have the ability to alter the composition of their membranes in response to temperature in ways that facilitate resource uptake (high temperatures) or increase respiratory efficiency (low temperatures; Hall et al 2010). …”

Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection

“…While the individual stability indicates the importance of host genotype for the community assembly , the fine-scale differences between the treatments also illustrate acclimation potential of the hemolmyph microbiome. Multiple competing ecotypes usually coexist in bacterial populations (Cohan and Koeppel, 2008) and even the isolates with virtually identical 16s rRNA sequences are sometimes adapted to very different conditions (Cohan and Koeppel, 2008;Hall et al, 2010), We cannot determine bacterial activity (Campbell et al, 2011) nor function (Salles et al, 2012) based on 16s rDNA sequences; moreover, our coverage is insufficient to capture very rare bacteria and thus estimate the full potential for community acclimation (Sjostedt et al, 2012). Nevertheless, relatively high persistence of bacterial residents and the adjustments in fine-scale community composition following the environmental change could represent the microbiome's way to buffer the impact of environmental stress.…”