Who Ate Whom? Adaptive Helicobacter Genomic Changes That Accompanied a Host Jump from Early Humans to Large Felines

Abstract

Helicobacter pylori infection of humans is so old that its population genetic structure reflects that of ancient human migrations. A closely related species, Helicobacter acinonychis, is specific for large felines, including cheetahs, lions, and tigers, whereas hosts more closely related to humans harbor more distantly related Helicobacter species. This observation suggests a jump between host species. But who ate whom and when did it happen? In order to resolve this question, we determined the genomic sequence of H. acinonychis strain Sheeba and compared it to genomes from H. pylori. The conserved core genes between the genomes are so similar that the host jump probably occurred within the last 200,000 (range 50,000–400,000) years. However, the Sheeba genome also possesses unique features that indicate the direction of the host jump, namely from early humans to cats. Sheeba possesses an unusually large number of highly fragmented genes, many encoding outer membrane proteins, which may have been destroyed in order to bypass deleterious responses from the feline host immune system. In addition, the few Sheeba-specific genes that were found include a cluster of genes encoding sialylation of the bacterial cell surface carbohydrates, which were imported by horizontal genetic exchange and might also help to evade host immune defenses. These results provide a genomic basis for elucidating molecular events that allow bacteria to adapt to novel animal hosts.

How old are bacterial pathogens?

“…The only known natural hosts for H. pylori are humans, but these bacteria can also infect some laboratory animals and are transmitted from humans to captive primates in zoos. Helicobacter acinonychis, the closest relative of H. pylori, seems to have arisen as a distinct species after a host jump of H. pylori from humans to large felines [18]. In the late 1990s, I became intrigued by why the genetic diversity of H. pylori seemed to reflect their geographical origins [19].…”

Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens

“…Complete genome sequences have been determined for three Helicobacter species (five different strains in total) (12,(14)(15)(16)(17), three strains of Campylobacter jejuni (13,18) and an additional five Campylobacter strains (18). Complete genome sequences and comparative genomic analysis of these pathogenic -Proteobacteria have provided important insights into their virulence factors, habitat specificities, and mechanisms of initial colonization, as well as into the significant genome plasticity (15)(16)(17)(18)(19)(20). Wolinella succinogenes DSM1740 T is the only nonpathogenic, host (cattle)-adapted -proteobacterium for which a complete genome sequence is available (21).…”

Phylogeny vs genome reshuffling: horizontal gene transfer

“…Variably present gene may refl ect host-adaptation processes and give hints to the differences in lifestyle and host preferences [126]. Reduction in Helicobacter pylori and H. acinonychis genome sizes compared to H. hepaticus has been suggested as a result of a host adaptation process following a host jump [127]. The presence of a large number of genome islands indicates a large fl exible gene pool for this group of bacteria.…”