Analysis of twelve genomes of the bacterium Kerstersia gyiorum from brown-throated sloths (Bradypus variegatus), the first from a non-human host

Dennis Carhuaricra-Huaman; Irys H L Gonzalez; Patricia L Ramos; Aline M da Silva; Joao C Setubal

doi:10.7717/peerj.17206

Analysis of twelve genomes of the bacterium Kerstersia gyiorum from brown-throated sloths (Bradypus variegatus), the first from a non-human host

PeerJ. 2024 Apr 4:12:e17206. doi: 10.7717/peerj.17206. eCollection 2024.

Authors

Dennis Carhuaricra-Huaman¹, Irys H L Gonzalez², Patricia L Ramos², Aline M da Silva¹, Joao C Setubal¹

Affiliations

¹ Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, SP, Brazil.
² Coordenadoria de Fauna Silvestre, Secretaria do Meio Ambiente, São Paulo, SP, Brazil.

Abstract

Kerstersia gyiorum is a Gram-negative bacterium found in various animals, including humans, where it has been associated with various infections. Knowledge of the basic biology of K. gyiorum is essential to understand the evolutionary strategies of niche adaptation and how this organism contributes to infectious diseases; however, genomic data about K. gyiorum is very limited, especially from non-human hosts. In this work, we sequenced 12 K. gyiorum genomes isolated from healthy free-living brown-throated sloths (Bradypus variegatus) in the Parque Estadual das Fontes do Ipiranga (São Paulo, Brazil), and compared them with genomes from isolates of human origin, in order to gain insights into genomic diversity, phylogeny, and host specialization of this species. Phylogenetic analysis revealed that these K. gyiorum strains are structured according to host. Despite the fact that sloth isolates were sampled from a single geographic location, the intra-sloth K. gyiorum diversity was divided into three clusters, with differences of more than 1,000 single nucleotide polymorphisms between them, suggesting the circulation of various K. gyiorum lineages in sloths. Genes involved in mobilome and defense mechanisms against mobile genetic elements were the main source of gene content variation between isolates from different hosts. Sloth-specific K. gyiorum genome features include an IncN2 plasmid, a phage sequence, and a CRISPR-Cas system. The broad diversity of defense elements in K. gyiorum (14 systems) may prevent further mobile element flow and explain the low amount of mobile genetic elements in K. gyiorum genomes. Gene content variation may be important for the adaptation of K. gyiorum to different host niches. This study furthers our understanding of diversity, host adaptation, and evolution of K. gyiorum, by presenting and analyzing the first genomes of non-human isolates.

Keywords: Brown-throated sloths; CRISPR-Cas; Genomics; Host-specific genes; IncN2 plasmid; Kerstersia gyiorum; Mobile genetic elements; Pangenome; Phylogenomics.

MeSH terms

Alcaligenaceae* / genetics
Animals
Brazil
Phylogeny
Sloths* / genetics

Supplementary concepts

Kerstersia gyiorum

Grants and funding

The work (proposal: 10.46936/10.25585/60001079) was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. This work was also funded by grant 2011/50870-6 from the São Paulo State Research Foundation (FAPESP). Aline M da Silva and Joao C Setubal received Research Fellowship Awards from the National Council for Scientific and Technological Development (CNPq). There were no other external funding sources. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.