Ecophysiological Features Shape the Distribution of Prophages and CRISPR in Sulfate Reducing Prokaryotes

Abstract

Sulfate reducing prokaryotes (SRP) are a phylogenetically and physiologically diverse group of microorganisms that use sulfate as an electron acceptor. SRP have long been recognized as key players of the carbon and sulfur cycles, and more recently, they have been identified to play a relevant role as part of syntrophic and symbiotic relations and the human microbiome. Despite their environmental relevance, there is a poor understanding about the prevalence of prophages and CRISPR arrays and how their distribution and dynamic affect the ecological role of SRP. We addressed this question by analyzing the results of a comprehensive survey of prophages and CRISPR in a total of 91 genomes of SRP with several genotypic, phenotypic, and physiological traits, including genome size, cell volume, minimum doubling time, cell wall, and habitat, among others. Our analysis discovered 81 prophages in 51 strains, representing the 56% of the total evaluated strains. Prophages are non-uniformly distributed across the SRP phylogeny, where prophage-rich lineages belonged to Desulfovibrionaceae and Peptococcaceae. Furthermore, our study found 160 CRISPR arrays in 71 SRP, which is more abundant and widely spread than previously expected. Although there is no correlation between presence and abundance of prophages and CRISPR arrays at the strain level, our analysis showed that there is a directly proportional relation between cellular volumes and number of prophages per cell. This result suggests that there is an additional selective pressure for strains with smaller cells to get rid of foreign DNA, such as prophages, but not CRISPR, due to less availability of cellular resources. Analysis of the prophage genes encoding viral structural proteins reported that 44% of SRP prophages are classified as Myoviridae, and comparative analysis showed high level of homology, but not synteny, among prophages belonging to the Family Desulfovibrionaceae. We further recovered viral-like particles and structures that resemble outer membrane vesicles from D. vulgaris str. Hildenborough. The results of this study improved the current understanding of dynamic interactions between prophages and CRISPR with their hosts in both cultured and hitherto-uncultured SRP strains, and how their distribution affects the microbial community dynamics in several sulfidogenic natural and engineered environments.

Exploring how the fast-slow pace of life continuum and reproductive strategies structure microorganism life history variation

“…Polytomies were collapsed using the function multi2di in ape [55]. Copiotroph and oligotroph classification was according to Stone et al 2023 for species 2-10, and suspected classifications (indicated with questions marks) are from [58] (species 2), [59] (species 11), and [60] (species 12-13).…”

“…Values in (A) are the scores of p-PC1 and values in (B) are the scores of p-PC2 (Fig. 2A).Copiotroph and oligotroph classification was according to[58] (species 1),[5] (species 2-10),[59] (species 11), and[60] (species 12-13) (questions marks indicate suspected classifications).…”

Clustered Regularly Interspaced Short Palindromic Repeat/CRISPR-Associated Protein and Its Utility All at Sea: Status, Challenges, and Prospects

“…Some phylogenetically diverse functional groups have a high prevalence of CRISPR/Cas. For instance, a comparative analysis of 91 sulfate-reducing prokaryote (SRP) genomes revealed the existence of CRISPR/Cas systems in as many as 78% of taxa [ 53 ]. This frequency is remarkably higher than in other reported prokaryotes.…”

Temperate bacteriophage induced inPseudomonas aeruginosabiofilms can modulate bacteriophage and antibiotic resistance

“…Prophages are increasingly recognized as an important component in the complex interplay between host, pathogen and environment associated with CF (9)(10)(11).…”