Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers

Abstract

SummaryReverse gyrase, an enzyme of uncertain funtion, is present in all hyperthermophilic archaea and bacteria. Previous phylogenetic studies have suggested that the gene for reverse gyrase has an archaeal origin and was transferred laterally (LGT) to the ancestors of the two bacterial hyperthermophilic phyla, Thermotogales and Aquificales. Here, we performed an in-depth analysis of the evolutionary history of reverse gyrase in light of genomic progress. We found genes coding for reverse gyrase in the genomes of several thermophilic bacteria that belong to phyla other than Aquificales and Thermotogales. Several of these bacteria are not, strictly speaking, hyperthermophiles because their reported optimal growth temperatures are below 80°C. Furthermore, we detected a reverse gyrase gene in the sequence of the large plasmid of Thermus thermophilus strain HB8, suggesting a possible mechanism of transfer to the T. thermophilus strain HB8 involving plasmids and transposases. The archaeal part of the reverse gyrase tree is congruent with recent phylogenies of the archaeal domain based on ribosomal proteins or RNA polymerase subunits. Although poorly resolved, the complete reverse gyrase phylogeny suggests an ancient acquisition of the gene by bacteria via one or two LGT events, followed by its secondary distribution by LGT within bacteria. Finally, several genes of archaeal origin located in proximity to the reverse gyrase gene in bacterial genomes have bacterial homologues mostly in thermophiles or hyperthermophiles, raising the possibility that they were co-transferred with the reverse gyrase gene. Our new analysis of the reverse gyrase history strengthens the hypothesis that the acquisition of reverse gyrase may have been a crucial evolutionary step in the adaptation of bacteria to high-temperature environments. However, it also questions the role of this enzyme in thermophilic bacteria and the selective advantage its presence could provide.

The origin of modern terrestrial life

“…In our opinion, a mesophilic LUCA fits better with the observation that hyperthermophiles are sophisticated organisms that have evolved specific mechanisms to thrive at very high temperatures [for a review see (Forterre and Philippe, 1999a;Xu and Glansdorff, 2002)]. In particular, phylogenomics analyses indeed suggest that reverse gyrase, an atypical DNA topoisomerase present in all hyperthermophiles, was absent in LUCA (Brochier-Armanet and Forterre, 2006;Forterre et al, 2000) whereas hot-temperature-adapted lipids are not homologous in Archaea and Bacteria, suggesting a secondary adaptation that occurred independently in each of these domains (Forterre and Philippe, 1999a;Xu and Glansdorff, 2002).…”

Separate and Combined Biochemical Activities of the Subunits of a Naturally Split Reverse Gyrase

“…Since its discovery in a hyperthermophilic archaeon (7), there is growing evidence suggesting a role of reverse gyrase in stabilizing genomes in hyperthermophiles. It appears to be the only gene specific to hyperthermophiles (8) and is present in all hyperthermophiles and in some thermophiles as well (9). This unique function of reverse gyrase is further supported by genetic evidence.…”

“…Although the biochemical mechanism for directional strand transfer remains unclear, the structural biological and biochemical studies on the enzyme provide important insight. Reverse gyrase is composed of a superfamily II helicase-like domain at its N-terminal half linked to a type IA topoisomerase domain (9,14). The crystal structure of Archaeoglobus fulgidus reverse gyrase indicates that these domains are arranged back-to-back with the active site of each domain facing away from its counterpart (15,16).…”

“…Instead, further analysis of its genome reveals two separate genes encoding the apparent topoisomerase IA and helicaselike domains of reverse gyrase (9,20). This raises the possibility that what in other hyperthermophiles are two domains of a single peptide, in N. equitans are distinct subunits of a multiprotein complex.…”

DNA-DNA Recognition: From Tight Contact to Fatal Attraction

“…Indeed, in contrast to life at high temperature that can tolerate various topological states of DNA -from negative supercoiled DNA to slightly positively supercoiled DNA-(BrochierArmanet and Forterre, 2006;Charbonnier and Forterre, 1994;Guipaud et al, 1997;LopezGarcia et al, 2000;Marguet and Forterre, 1994), adaptation to mesophilic life is much more contraining on the topology of DNA: the genome of mesophilic organisms, including bacteria, archaea and eukarya, is systematically (-) supercoiled. All mesophilic bacteria have a DNA gyrase that introduce (-) supercoiling in a plectonemic form (Forterre and Gadelle, 2009).…”