Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis

Abstract

A plethora of pathogenic viruses colonize bats. However, bat bacterial flora and its zoonotic threat remain ill defined. In a study initially conducted as a quantitative metagenomic analysis of the fecal bacterial flora of the Daubenton's bat in Finland, we unexpectedly detected DNA of several hemotrophic and ectoparasite-transmitted bacterial genera, including Bartonella. Bartonella spp. also were either detected or isolated from the peripheral blood of Daubenton's, northern, and whiskered bats and were detected in the ectoparasites of Daubenton's, northern, and Brandt's bats. The blood isolates belong to the Candidatus-status species B. mayotimonensis, a recently identified etiologic agent of endocarditis in humans, and a new Bartonella species (B. naantaliensis sp. nov.). Phylogenetic analysis of bat-colonizing Bartonella spp. throughout the world demonstrates a distinct B. mayotimonensis cluster in the Northern Hemisphere. The findings of this field study highlight bats as potent reservoirs of human bacterial pathogens.

Keywords: Bartonella; Northern Hemisphere; bacteria; bats; endocarditis; metagenomics.

Figure 1

Quantitative metagenomic analysis of the fecal DNA of the Daubenton’s bat. The sequences (>50 bp) were assigned on the basis of best E-value BLASTN scores (http://blast.ncbi.nlm.nih.gov/blast.cgi) in GenBank. Numbers refer to the amount of sequences assigned to a given taxon. No hits refers to sequences that had no similarity to any sequences in GenBank. Not assigned refers to sequences that had similarity in GenBank but they could not be reliably assigned to any organism. Arrows mark the ectoparasite-transmitted bacterial genera, which unexpectedly were detected in the bat fecal DNA preparation.

Figure 2

Phylogenetic positions of the bat blood isolates among members of the genus Bartonella. Neighbor-joining (A) and maximum-likelihood (B) trees are based on the alignment of concatenated sequences of 4 multilocus sequence analysis markers (rpoB, gltA, 16S rRNA, and ftsZ). Sequence information from the type strains of all known Bartonella species and from the Candidatus B. mayotimonensis human strain was included into the analysis (Technical Appendix Table 5). Numbers on branches indicate bootstrap support values derived from 1,000 tree replicas. Bootstrap values >60 are shown. Scale bar indicates nucleotide substitutions per site.

Figure 3

Phylogenetic analysis of bat-colonizing Bartonella spp. found worldwide demonstrates a distinct B. mayotimonensis cluster in the Northern Hemisphere. Maximum composite likelihood–based neighbor-joining tree is based on the alignment of the gltA multilocus sequence analysis marker. Information from Bartonella gltA sequences from bat blood isolates or from minced tissues of bats or from bat ectoparasites was included in the analysis. GenBank accession numbers of the sequences are shown after the country of origin. Numbers on branches indicate bootstrap support values derived from 1,000 tree replicas. Bootstrap values >60 are shown. Scale bar indicates nucleotide substitutions per site.