Horizontal gene transfer and CRISPR targeting drive phage-bacterial host interactions and coevolution in pink berry marine microbial aggregates

Abstract

Bacteriophages (phages), viruses that infect bacteria, are the most abundant components of microbial communities and play roles in community dynamics and host evolution. The study of phage-host interactions, however, is made difficult by a paucity of model systems from natural environments and known and cultivable phage-host pairs. Here, we investigate phage-host interactions in the "pink berry" consortia, naturally-occurring, low-diversity, macroscopic aggregates of bacteria found in the Sippewissett Salt Marsh (Falmouth, MA, USA). We leverage metagenomic sequence data and a comparative genomics approach to identify eight compete phage genomes, infer their bacterial hosts from host-encoded clustered regularly interspaced short palindromic repeats (CRISPR), and observe the potential evolutionary consequences of these interactions. Seven of the eight phages identified infect the known pink berry symbiontsDesulfofustissp. PB-SRB1,Thiohalocapsasp. PB-PSB1, andRhodobacteraceaesp. A2, and belong to entirely novel viral taxa, except for one genome which represents the second member of theKnuthellervirusgenus. We further observed increased nucleotide variation over a region of a conserved phage capsid gene that is commonly targeted by host CRISPR systems, suggesting that CRISPRs may drive phage evolution in pink berries. Finally, we identified a predicted phage lysin gene that was horizontally transferred to its bacterial host, potentially via a transposon intermediary, emphasizing the role of phages in bacterial evolution in pink berries. Taken together, our results demonstrate that pink berry consortia contain diverse and variable phages, and provide evidence for phage-host co-evolution via multiple mechanisms in a natural microbial system.

Viromes vs. mixed community metagenomes: choice of method dictates interpretation of viral community ecology

“…Viral genomes are very heterogeneous and mosaic, and viruses overall exhibit significant intra-population variation on the nucleotide level as well as on a gene-by-gene basis [4,86–91]. Consequently, if the overall viral community composition inferred from viromes is different than that of metagenomes, we reasoned that we would also see a difference on the protein-coding gene-level.…”

“…Viruses exist in all known ecosystems and infect cells from all domains of life. Being the most abundant biological entity on Earth [1,2], viruses significantly impact the ecology and evolution of their hosts [3,4], play pivotal roles in microbial community succession [5], contribute to community-wide metabolic processes [6–8], and are a source of novel therapies being used to combat a worldwide antimicrobial resistance crisis [9,10]. Advances in these areas have been enabled by large-scale investigations into entire communities of viruses which have revealed tremendous amounts of previously unknown virus diversity in human [11–13] and environmental [14–18] systems.…”

Dynamics of CRISPR-mediated virus-host interactions in the human gut microbiome

“…Some recurrent findings of previous studies are: (i) long-term coexistence of MGE with a polymorphic population of hosts that includes immune and sensitive lineages; (ii) high levels of local adaptation in the host CRISPR arrays; and (iii) high frequency of mutations in regions of MGE targeted by CRISPR spacers. Coexistence of MGE and host lineages is generally interpreted in terms of the diversity-promoting effects of clonal interference and herd immunity (27)(28)(29)(30)(31), whereas coevolution of CRISPR and MGE suggests that CRISPR-Cas is functional and the selective pressure that it imposes on MGE is strong enough to fuel mutational escape (32,33). Interestingly, these conclusions may not extend to host-associated microbiomes.…”

Critical analysis of polycyclic tetramate macrolactam biosynthetic cluster phylogeny and functional diversity

“…In terms of producer phylogeny, these efforts immediately expanded the catalog of putative PTM producers into the actinobacterial genera Actinophytocola , Amycolatopsis, Thermomonospora, and Streptosporangium. Several new proteobacterial producers were also identified including Chitinimonas , plus several metagenome assembled genomes (MAG) including Cellvibrio from citrus rhizosphere (43) , Thiohalocapsa from a ‘pink berry’ sulfur cycling consortium (44–46), and a putative Myxococcales bacterium found in wastewater sludge (47) (Fig S2).…”