Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae

Abstract

Thermophiles are extremophiles that grow optimally at temperatures >45°C. To survive and maintain function of their biological molecules, they have a suite of characteristics not found in organisms that grow at moderate temperature (mesophiles). At the cellular level, thermophiles have mechanisms for maintaining their membranes, nucleic acids, and other cellular structures. At the protein level, each of their proteins remains stable and retains activity at temperatures that would denature their mesophilic homologs. Conversely, cellular structures and proteins from thermophiles may not function optimally at moderate temperatures. These differences between thermophiles and mesophiles presumably present a barrier for evolutionary transitioning between the 2 lifestyles. Therefore, studying closely related thermophiles and mesophiles can help us determine how such lifestyle transitions may happen. The bacterial phylum Thermotogae contains hyperthermophiles, thermophiles, mesophiles, and organisms with temperature ranges wide enough to span both thermophilic and mesophilic temperatures. Genomic, proteomic, and physiological differences noted between other bacterial thermophiles and mesophiles are evident within the Thermotogae. We argue that the Thermotogae is an ideal group of organisms for understanding of the response to fluctuating temperature and of long-term evolutionary adaptation to a different growth temperature range.Key words: lateral gene transfer, Kosmotoga, Mesotoga, thermostability, stress response. Résumé :Les thermophiles sont des extrémophiles dont la température optimale de croissance se situe au-delà de 45°C. Pour survivre et permettre à leurs biomolécules de bien fonctionner, ils doivent se doter de caractéristiques qu'on ne retrouve pas chez des organismes se développant à des températures intermédiaires (mésophiles). Sur le plan cellulaire, les thermophiles ont des mécanismes permettant de préserver leurs membranes, acides nucléiques et autres structures cellulaires. Au chapitre des protéines, chacune d'entre elles demeure stable et active à des températures qui dénatureraient leurs homologues mésophiles. En revanche, les structures et protéines cellulaires des thermophiles pourraient ne pas fonctionner de manière optimale à des températures intermédiaires. De telles différences entre les thermophiles et les mésophiles auraient tendance à se dresser en travers d'une transition évolutive entre ces deux modes de vie. Par conséquent, l'étude de thermophiles et de mésophiles fortement apparentés pourrait nous permettre d'établir comment surviendraient de telles transitions du mode de vie. Le phylum bactérien Thermotogae regroupe des hyperthermophiles, des thermophiles, des mésophiles et des organismes dont l'intervalle de températures chevauche les plages thermophiles et mésophiles. On observe parmi les Thermotogae des différences sur le plan génomique, protéomique, et physiologique qu'on relève également entre d'autres thermophiles et méso-philes bactériens. Nous soutenons que les Thermot...

Genomic analysis of the mesophilic Thermotogae genus Mesotoga reveals phylogeographic structure and genomic determinants of its distinct metabolism

“…However, it is unclear how growth temperature affects other aspects of genome evolution including levels of homologous recombination. Hyperthermophilic Thermotoga display extremely high levels of homologous recombination, which could be a side effect of the need for DNA repair at high temperatures (Nesbø et al, 2015). Nesbø et al (2015) also found high levels of geneflow among all Thermotoga spp.…”

“…Hyperthermophilic Thermotoga display extremely high levels of homologous recombination, which could be a side effect of the need for DNA repair at high temperatures (Nesbø et al, 2015). Nesbø et al (2015) also found high levels of geneflow among all Thermotoga spp. genomes investigated, and that populations from similar environments have exchanged more genes than geographically close populations from different environments.…”

“…The genus Mesotoga is the only characterized mesophilic lineage within the otherwise thermophilic bacterial phylum Thermotogae (Pollo et al, 2015). Mesotoga spp.…”

“…Genome size in Thermotogae inversely correlates with optimum growth temperature (Zhaxybayeva et al, 2012;Pollo et al, 2015). However, it is unclear how growth temperature affects other aspects of genome evolution including levels of homologous recombination.…”

“…For instance, Thermotoga genomes from oil reservoirs in Japan and in the North Sea, as well as from a continental hot spring in North America, have exchanged more genes through homologous recombination than they have with genomes from geographically closer marine vents. Moreover, the phylogeographic analysis of Thermotoga genomes suggested that oil reservoirs were colonized from subsurface populations rather than being buried with the sediments that mature into oil reservoirs (a corollary of the paleosterilization hypothesis; Wilhelms et al, 2001) (Nesbø et al, 2015). Comparative genomic analyses of mesophilic Thermotogae may shed light on the role of growth temperature on recombination and phylogeography.…”