Correction: The Biokinetic Spectrum for Temperature.

[This corrects the article DOI: 10.1371/journal.pone.0153343.].

The Biokinetic Spectrum for Temperature.

We identify and describe the distribution of temperature-dependent specific growth rates for life on Earth, which we term the biokinetic spectrum for temperature. The spectrum has the potential to provide for more robust modeling in thermal ecology since any conclusions derived from it will be based on observed data rather than using theoretical assumptions. It may also provide constraints for systems biology model predictions and provide insights in physiology. The spectrum has a Δ-shape with a sharp peak at around 42°C. At higher temperatures up to 60°C there was a gap of attenuated growth rates. We found another peak at 67°C and a steady decline in maximum rates thereafter. By using Bayesian quantile regression to summarise and explore the data we were able to conclude that the gap represented an actual biological transition between mesophiles and thermophiles that we term the Mesophile-Thermophile Gap (MTG). We have not identified any organism that grows above the maximum rate of the spectrum. We used a thermodynamic model to recover the Δ-shape, suggesting that the growth rate limits arise from a trade-off between activity and stability of proteins. The spectrum provides underpinning principles that will find utility in models concerned with the thermal responses of biological processes.

Protein thermodynamics can be predicted directly from biological growth rates.

Life on Earth is capable of growing from temperatures well below freezing to above the boiling point of water, with some organisms preferring cooler and others hotter conditions. The growth rate of each organism ultimately depends on its intracellular chemical reactions. Here we show that a thermodynamic model based on a single, rate-limiting, enzyme-catalysed reaction accurately describes population growth rates in 230 diverse strains of unicellular and multicellular organisms. Collectively these represent all three domains of life, ranging from psychrophilic to hyperthermophilic, and including the highest temperature so far observed for growth (122 °C). The results provide credible estimates of thermodynamic properties of proteins and obtain, purely from organism intrinsic growth rate data, relationships between parameters previously identified experimentally, thus bridging a gap between biochemistry and whole organism biology. We find that growth rates of both unicellular and multicellular life forms can be described by the same temperature dependence model. The model results provide strong support for a single highly-conserved reaction present in the last universal common ancestor (LUCA). This is remarkable in that it means that the growth rate dependence on temperature of unicellular and multicellular life forms that evolved over geological time spans can be explained by the same model.

Variation of branched-chain fatty acids marks the normal physiological range for growth in Listeria monocytogenes.

The fatty acid composition of Listeria monocytogenes Scott A was determined by close-interval sampling over the entire biokinetic temperature range. There was a high degree of variation in the percentage of branched-chain fatty acids at any given temperature. The percentage of branched C17 components increased with growth temperature in a linear manner. However, the percentages of iso-C15:0 (i15:0) and anteiso-C15:0 (a15:0) were well described by third-order and second-order polynomial curves, respectively. There were specific temperature regions where the proportion of branched-chain fatty acids deviated significantly from the trend established over the entire growth range. In the region from 12 to 13 degrees C there were significant deviations in the percentages of both i15:0 and a15:0 together with a suggested deviation in a17:0, resulting in a significant change in the total branched-chain fatty acids. In the 31 to 33 degrees C region the percentage of total branched-chain components exhibited a significant deviation. The observed perturbations in fatty acid composition occurred near the estimated boundaries of the normal physiological range for growth.

Biomarker techniques to screen for bacteria that produce polyunsaturated fatty acids.

The production of polyunsaturated fatty acids (PUFA) by bacteria has been firmly established for over two decades although it is still commonly ignored. Investigations of Antarctic sea ice have revealed a high diversity of novel bacterial taxa with the ability to produce PUFA. The majority are psychrophilic (requiring low temperatures for growth) and halophilic (requiring the presence of salts for growth), in contrast to the bacterial community present in the underlying water column. Specific fatty acids may be used as indicators of PUFA-producing bacteria in environmental samples. Structural studies of bacterial phospholipids have been particularly revealing in suggesting biomarkers specific for prokaryotic PUFA input. The use of negative ion fast atom bombardment tandem mass spectrometry for the analysis of bacterial phospholipids has identified species specific for certain groups of bacterial PUFA producers. The phylogeny of PUFA production in the gamma-Proteobacteria also suggests the future use of PUFA genes for the assessment of marine bacterial biodiversity.

Psychroflexus torquis gen. nov., sp. nov., a psychrophilic species from Antarctic sea ice, and reclassification of Flavobacterium gondwanense (Dobson et al. 1993) as Psychroflexus gondwanense gen. nov., comb. nov.

A group of sea-ice-derived psychrophilic bacterial strains possessing the unusual ability to synthesize the polyunsaturated fatty acids eicosapentaenoic acid (20:5 omega 3) and arachidonic acid (20:4 omega 6) belong to the Family Flavobacteriaceae (Flexibacter-Bacteroides-Flavobacterium phylum), according to 16S rRNA sequence analysis. Surprisingly, the isolates were also found to cluster closely to the moderately halophilic and psychrotrophic species [Flavobacterium] gondwanense (sequence similarity 97.8-98.1%). The whole-cell fatty acid profiles of this group and [Flavobacterium] gondwanense were very similar and distinct from other related flavobacteria. The sea ice strains and [Flavobacterium] gondwanense differed substantially in terms of ecophysiology, possibly representing divergent adaptations to sympagic and planktonic marine habitats, respectively. Evidence based on phylogeny and fatty acid profiles supports the conclusion that the taxa are close relatives distinct from other bacterial groups. It is thus proposed that the sea ice strains represent a novel taxon designated Psychroflexus torquis gen. nov., sp. nov. (type strain ACAM 623T) while [Flavobacterium] gondwanense becomes Psychroflexus gondwanense gen. nov., comb. nov.