Genomic analysis of group B Streptococcus from milk demonstrates the need for improved biosecurity: a cross-sectional study of pastoralist camels in Kenya

Abstract

Background: Streptococcus agalactiae (Group B Streptococcus, (GBS)) is the leading cause of mastitis (inflammation of the mammary gland) among dairy camels in Sub-Saharan Africa, with negative implications for milk production and quality and animal welfare. Camel milk is often consumed raw and presence of GBS in milk may pose a public health threat. Little is known about the population structure or virulence factors of camel GBS. We investigated the molecular epidemiology of camel GBS and its implications for mastitis control and public health.

Results: Using whole genome sequencing, we analysed 65 camel milk GBS isolates from 19 herds in Isiolo, Kenya. Six sequence types (STs) were identified, mostly belonging to previously described camel-specific STs. One isolate belonged to ST1, a predominantly human-associated lineage, possibly as a result of interspecies transmission. Most (54/65) isolates belonged to ST616, indicative of contagious transmission. Phylogenetic analysis of GBS core genomes showed similar levels of heterogeneity within- and between herds, suggesting ongoing between-herd transmission. The lactose operon, a marker of GBS adaptation to the mammary niche, was found in 75 % of the isolates, and tetracycline resistance gene tet(M) in all but two isolates. Only the ST1 isolate harboured virulence genes scpB and lmb, which are associated with human host adaptation.

Conclusions: GBS in milk from Kenyan camel herds largely belongs to ST616 and shows signatures of adaptation to the udder. The finding of similar levels of within- and between herd heterogeneity of GBS in camel herds, as well as potential human-camel transmission highlights the need for improved internal as well as external biosecurity to curb disease transmission and increase milk production.

Keywords: Biosecurity; Camelids; Dairy; Intramammary infection; Molecular epidemiology; Nomadic; Streptococcus agalactiae.

Fig. 1

Flowchart of sample and mastitis classification: normal milk (CMT < 3), mastitis (defined as a CMT-score ≥ 3), subclinical mastitis (defined as a CMT- score ≥ 3 and no palpatory or visual changes of the udder or milk), clinical mastitis (defined as CMT-score ≥ 3 and abnormalities in the milk or udder), acute clinical mastitis (ACM) (defined as a CMT-score ≥ 3 and swelling, pain, redness or abnormal milk), and chronic clinical mastitis (CCM) (defined as a CMT-score ≥ 3 and induration of the udder)

Fig. 2

Maximum likelihood phylogenetic tree based on a core genome alignment of 65 camel group B Streptococcus (GBS) isolates. Leaf colours correspond to herd of origin (n = 19), whose locations are indicated on the map. Sequence types (ST) are shown on the branches, with the ST616 nomenclature also comprising its two single locus variants (ST1653 and ST1654). Grey bars indicate Lac.2 genotypic variants. A single genome assembly belonging to ST1 was removed from the tree to facilitate visualisation. Tree has been rooted at midpoint. ILRI112 (ST617; accession HF952106) was used as reference genome. The map was created with ggplot in RStudio, with R (v4.0.)

Fig. 3

Frequency distribution of pairwise genetic distances calculated between genomes from the largest group B Streptococcus lineage from camel milk (sequence types 616, 1653 and 1654) belonging to the same herd (within-herd diversity) or to different herds (between-herd diversity)