Host adaptation in gut Firmicutes is associated with sporulation loss and altered transmission cycle

Abstract

Background 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. The Firmicutes are a dominant phylum within the intestinal microbiota that are capable of producing resistant endospores that maintain viability within the environment and germinate within the intestine to facilitate transmission. However, the impact of host transmission on the evolutionary and adaptive processes within the intestinal microbiota remains unknown. Results We analyze 1358 genomes of Firmicutes bacteria derived from host and environment-associated habitats. Characterization of genomes as spore-forming based on the presence of sporulation-predictive genes reveals multiple losses of sporulation in many distinct lineages. Loss of sporulation in gut Firmicutes is associated with features of host-adaptation such as genome reduction and specialized metabolic capabilities. Consistent with these data, analysis of 9966 gut metagenomes from adults around the world demonstrates that bacteria now incapable of sporulation are more abundant within individuals but less prevalent in the human population compared to spore-forming bacteria. Conclusions Our results suggest host adaptation in gut Firmicutes is an evolutionary trade-off between transmission range and colonization abundance. We reveal host transmission as an underappreciated process that shapes the evolution, assembly, and functions of gut Firmicutes.

Mechanisms and Applications of Bacterial Sporulation and Germination in the Intestine

“…Kearney et al showed that lysozyme resistant bacteria are more likely to be shared among multiple individuals, which suggest that these costly resistant states are beneficial for cross-host transmission [ 10 ]. In line with this, Browne et al recently found that loss of the ability to sporulate led to greater relative abundance within an individual host, but lower overall prevalence in the population [ 127 ]. Thus, spore-forming bacteria may have lower colonization capacity within a specific niche but are capable of much greater host to host transmission, due to their survival strategy, environmental adaptability, and metabolic capabilities, than more specialized asporogenous species [ 127 ].…”

“…As discussed above, bile acids are germinants, which might indicate that spore forming species have evolved as inhabitants of the intestine by adapting to bile salts for germination in the intestine. Loss of sporulation genes within large taxonomic orders can be traced back to groups such as Lactobacillales and Staphylococcae [ 13 ] and this loss may be linked to bacterial adaptation to nutrient rich environments, allowing for greater growth by discarding expensive sporulation genes [ 127 ]. Interestingly, in the study conducted by Browne et al, loss of sporulation was observed least in the gut environment, as compared to soil, the rumen, and human oral sites, affirming that the ability to sporulate and germinate in the intestinal environment is advantageous in fecal–oral transmission [ 127 ].…”

“…Loss of sporulation genes within large taxonomic orders can be traced back to groups such as Lactobacillales and Staphylococcae [ 13 ] and this loss may be linked to bacterial adaptation to nutrient rich environments, allowing for greater growth by discarding expensive sporulation genes [ 127 ]. Interestingly, in the study conducted by Browne et al, loss of sporulation was observed least in the gut environment, as compared to soil, the rumen, and human oral sites, affirming that the ability to sporulate and germinate in the intestinal environment is advantageous in fecal–oral transmission [ 127 ]. For a more detailed reviews about transmission routes and colonization within infants we refer to Browne et al, 2017 and Egan et al, 2021 [ 3 , 129 ].…”

Metagenomic strain detection with SameStr: identification of a persisting core gut microbiota transferable by fecal transplantation

“…We detected strain persistence for many of the same bacterial taxa, such as Bacteroides species, as previously reported based on temporal single nucleotide polymorphism (SNP) stability [ 43 ] and strain-resolved species-specific MAGs [ 19 ] in fecal metagenomes from healthy individuals. Persistence has been negatively correlated to the genetic capacity for oxygen tolerance and sporulation before [ 19 ] and, based on comparative genome analyses, the loss of sporulation has been genetically linked to typical features of host-adaptation, such as genome reduction and metabolic specialization [ 44 ], confirming our functional predictions for species that are frequently represented by persisting strains, as well as our concept of a persisting core gut microbiota of strict anaerobe, non-spore-forming bacteria in the healthy human gut. We also identified a surprising taxonomic association between strain persistence and engraftment, as strains with a high persistence rate in healthy individuals belonged to the same bacterial species as donor strains with a high engraftment rate in rCDI patients after FMT.…”

Host Species Adaptation of Obligate Gut Anaerobes Is Dependent on Their Environmental Survival

“…Accumulating evidence shows that there are biological consequences of different modes of environmental survival. Anaerobic spore-forming bacteria usually exhibit a high prevalence in their hosts which is, however, associated with low abundance [14][15][16]. If these bacteria are used for reconstitution of the gut microbiota as probiotics, then they have to be supplied continuously [17,18], which is likely to mimic their continuous environmental supply [8].…”