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.

SHARCGS, a fast and highly accurate short-read assembly algorithm for de novo genomic sequencing

“…bacterial species isolated from the stomach of large felines. The sequences of the H. acinonychis genome (1.55 Mbp) and of the H. acinonychis plasmid pHac1 (3661 bp) were determined recently with Sanger technology (Eppinger et al 2006). The H. acinonychis genome contains 38% GC and 90% coding regions (Eppinger et al 2006), and the total repeat content is 0.48% (7509 bp) according to RepeatMasker analysis.…”

“…The sequences of the H. acinonychis genome (1.55 Mbp) and of the H. acinonychis plasmid pHac1 (3661 bp) were determined recently with Sanger technology (Eppinger et al 2006). The H. acinonychis genome contains 38% GC and 90% coding regions (Eppinger et al 2006), and the total repeat content is 0.48% (7509 bp) according to RepeatMasker analysis. In detail, RepeatMasker found five reverse transcriptase homologs (340 bp, 0.02%), 14 small RNAs (932 bp, 0.06%), 10 simple repeats (760 bp, 0.05%), and 141 low-complexity regions (5479 bp, 0.35%).…”

Characterization of NikR-responsive promoters of urease and metal transport genes of Helicobacter mustelae

“…Using the previously described H. pylori high affinity NikR binding sites (Delany et al 2005;Ernst et al 2006;Dosanjh et al 2009) and the H. mustelae NikR operators in the ureA and ureA2 promoters, we redefined the consensus sequence to TRWYA-N 15 -TRWYA. This consensus sequence was used to search the intergenic regions from -198 to ?2 (relative to the first nucleotide of the annotated translational startcodon) of the H. pylori, H. acinonychis and H. hepaticus genome sequences (Tomb et al 1997;Suerbaum et al 2003;Eppinger et al 2006 Fig. 3 NikR controls ureAB and ureA2B2 transcription by sequence-specific direct binding to the H. mustelae ureA and ureA2 promoter regions.…”

“…Since the discovery of H. pylori, many other Helicobacter species have been identified, and it is now generally acknowledged that the gastric mucosa of most, if not all, mammals can be colonized by gastric Helicobacter species (Solnick and Schauer 2001). These non-pylori Helicobacter species may provide good animal models to study Helicobacter infection in their natural hosts (O'Rourke and Lee 2003) and comparative genomics may contribute in our understanding of host specificity (Eppinger et al 2006).…”

Helicobacter pylori Salvages Purines from Extracellular Host Cell DNA Utilizing the Outer Membrane-Associated Nuclease NucT

“…In this time, the bacterium has become reliant on its human host, and the resulting effects of this niche-specific evolutionary strategy can be seen in the metabolic machinery encoded by the bacterial genome. Similar to the genetic phenomenon observed in many intracellular bacterial commensals (7), pathogens (8), and parasites (9,10), bioinformatic studies show that gene loss has played a major role in the evolutionary history of H. pylori as well as other members of the epsilonproteobacteria (11,12). Missing pathway elements in the H. pylori genome indicate an adaptation from an early terrestrial ancestor to the human niche that may be the result of the bacterium obtaining its nutrients directly from its human host.…”