Brucella Genetic Variability in Wildlife Marine Mammals Populations Relates to Host Preference and Ocean Distribution

Abstract

Intracellular bacterial pathogens probably arose when their ancestor adapted from a free-living environment to an intracellular one, leading to clonal bacteria with smaller genomes and less sources of genetic plasticity. Still, this plasticity is needed to respond to the challenges posed by the host. Members of the Brucella genus are facultative-extracellular intracellular bacteria responsible for causing brucellosis in a variety of mammals. The various species keep different host preferences, virulence, and zoonotic potential despite having 97–99% similarity at genome level. Here, we describe elements of genetic variation in Brucella ceti isolated from wildlife dolphins inhabiting the Pacific Ocean and the Mediterranean Sea. Comparison with isolates obtained from marine mammals from the Atlantic Ocean and the broader Brucella genus showed distinctive traits according to oceanic distribution and preferred host. Marine mammal isolates display genetic variability, represented by an important number of IS711 elements as well as specific IS711 and SNPs genomic distribution clustering patterns. Extensive pseudogenization was found among isolates from marine mammals as compared with terrestrial ones, causing degradation in pathways related to energy, transport of metabolites, and regulation/transcription. Brucella ceti isolates infecting particularly dolphin hosts, showed further degradation of metabolite transport pathways as well as pathways related to cell wall/membrane/envelope biogenesis and motility. Thus, gene loss through pseudogenization is a source of genetic variation in Brucella, which in turn, relates to adaptation to different hosts. This is relevant to understand the natural history of bacterial diseases, their zoonotic potential, and the impact of human interventions such as domestication.

Brucella Genomics: Macro and Micro Evolution

“…Wolbachia species and mitochondria are extreme genome reduction cases, in which genome streamlining promoted a permanent stage of endosymbiosis, with a high replication rate within the host environment [ 4 , 35 , 40 , 41 ]. Likewise, there are reports in gene decay on critical metabolic pathways in Brucella [ 27 , 42 ], and the chromosomal streamlining seems to have been an essential step in the separation from its closest relative, Ochrobactrum [ 3 , 43 ], as further detailed.…”

“…Following the increasing availability of Brucella WGS generated in the last decade and computational power to analyze these sequences [ 23 , 24 , 25 , 26 , 27 ], we have reviewed the variability of genetic traits concerning host preferences and the brucellae geographic origin.…”

Persistence of Brucella abortus lineages revealed by genomic characterization and phylodynamic analysis

“…The presence, orientation and distribution of 23 previously reported genomic islands (GI) or anomalous regions (regions likely acquired by horizontal gene transfer) [35][36][37] were examined across seven phylogenetically representative B. abortus genomes from CR. For this, a "genomic-island pseudo-molecule" was formed by concatenation of 23 genomic regions obtained from several Brucella reference sequences, as previously described [38]. A BLAST comparison between the representative genomes and the pseudo-molecule was performed and visualized using ACT (S1 Fig).…”

“…We wondered if the B. abortus lineages comprised more variation than that revealed by the SNP patterns used for the phylogenetic reconstruction. To asses this question, we looked at known genomic traits associated with variability in Brucella [37,38,44,45] that might explain PLOS NEGLECTED TROPICAL DISEASES PLOS NEGLECTED TROPICAL DISEASES phenotypic or pathogenic differences among the lineages. De novo assemblies of representative genomes from each lineage were produced to identify major changes in 23 GIs or anomalous regions.…”

Genome Sequences of Brucella Melitensis Strains QH2019001 and QH2019005 Provides Insight Into Different Evolutionary Origins Within Qinghai Province, China

“…Currently, the Brucella genus contains 11 accepted species, with 6 of those, namely, B. melitensis, B. abortus, B. suis, B. canis, B. ovis, and B. neotomae, considered 'classical' species [8]. While various species differ in host preference, virulence, and/or zoonotic potential, all Brucella species maintain a 97-99% genomic sequence identity [9].…”