Host adaptation in gut Firmicutes is associated with sporulation loss and altered colonisation patterns

Abstract

Human-to-human transmission of symbiotic, anaerobic bacteria is a fundamental evolutionary adaptation essential for membership of the human gut microbiota. However, despite its importance, the genomic and biological adaptations underpinning symbiont transmission remain poorly understood. Here, we show that sporulation ability, which promotes transmission of anaerobic bacteria, has been independently lost in many distinct evolutionary lineages of gut bacteria belonging to the Firmicutes phyla. Analysis of 1358 genome-sequenced Firmicutes reveals loss of sporulation is associated with features of host-adaptation such as genome reduction and specialized metabolic capabilities. Consistent with these data, analysis of 28,000 gut metagenomes from people around the world demonstrates that bacteria now incapable of sporulation are more abundant but less prevalent in the human population compared to spore-forming bacteria. Our results suggest host adaptation in gut Firmicutes is an evolutionary trade-off between transmission range and colonisation abundance, leading to distinct transmission cycles. We reveal host transmission as an underappreciated process that shapes the evolution, assembly and functions of gut Firmicutes.

The Sporobiota of the Human Gut

“…However, while the FSF genomes were more abundant in the gut, they were less prevalent across samples, indicating that a loss of sporulation ability limits the transmission of FSF bacteria. 50 …”

“…23,26,33,34 On the other hand, a recent publication by Browne et al investigated the loss of sporulation in the Firmicutes of the adult gut microbiome. 50 Genomes with a low sporulation signature score were designated as Former Spore-Formers (FSF), based on the belief that sporulation evolved just once in Firmicutes, while those with a high score were designated Spore-Formers (SF). 5,7,46 Genomes from the Lactobacillales order were entirely FSF, while in the Lachnospiraceae (described in more detail below), just 18% were FSF.…”

“…It has been suggested that their adaption to the nutrient-rich gut environment led to the loss of ability to form spores. 5,50 The sporobiota of the infant gut…”

Ecological Adaptations of Gut Microbiota Members and Their Consequences for Use as a New Generation of Probiotics

“…Non-spore-forming gut anaerobes are less likely to be found across multiple individuals than those capable of spore formation [ 48 ], and in agreement, host-dependent adaption of different species within genus Bacteroides has been described [ 67 ]. Bacteria no longer capable of sporulation are usually less prevalent but more abundant compared to spore-formers, suggesting an increase in colonization capacity [ 68 ]. Bacteroides species are vertically transferred from mothers to offspring, both in humans and chickens [ 24 , 61 ].…”

Bifidobacterium castoris strains isolated from wild mice show evidence of frequent host switching and diverse carbohydrate metabolism potential

“…Codiversification patterns have been linked to convergent acquisition of function by different bacterial phylogenetic clades, with horizontal gene transfer and gene loss proposed as potential mechanisms involved in the process (15,16). Furthermore, increased host-specificity has been suggested to be linked to reduced transmission capacity due to anaerobic and non-spore forming bacterial lifestyles (17,18).…”