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Comparative Genomics Provides Insight into the Function of Broad-Host Range Sponge Symbionts.

ABSTRACT: The fossil record indicates that the earliest evidence of extant marine sponges (phylum Porifera) existed during the Cambrian explosion and that their symbiosis with microbes may have begun in their extinct ancestors during the Precambrian period. Many symbionts have adapted to their sponge host, where they perform specific, specialized functions. There are also widely distributed bacterial taxa such as Poribacteria, SAUL, and Tethybacterales that are found in a broad range of invertebrate hosts. Here, we added 11 new genomes to the Tethybacterales order, identified a novel family, and show that functional potential differs between the three Tethybacterales families. We compare the Tethybacterales with the well-characterized Entoporibacteria and show that these symbionts appear to preferentially associate with low-microbial abundance (LMA) and high-microbial abundance (HMA) sponges, respectively. Within these sponges, we show that these symbionts likely perform distinct functions and may have undergone multiple association events, rather than a single association event followed by coevolution. IMPORTANCE Marine sponges often form symbiotic relationships with bacteria that fulfil a specific need within the sponge holobiont, and these symbionts are often conserved within a narrow range of related taxa. To date, there exist only three known bacterial taxa (Entoporibacteria, SAUL, and Tethybacterales) that are globally distributed and found in a broad range of sponge hosts, and little is known about the latter two. We show that the functional potential of broad-host range symbionts is conserved at a family level and that these symbionts have been acquired several times over evolutionary history. Finally, it appears that the Entoporibacteria are associated primarily with high-microbial abundance sponges, while the Tethybacterales associate with low-microbial abundance sponges.

SUBMITTER: Waterworth SC

PROVIDER: S-EPMC8546597 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Rhizoctonia solani is a soil-borne basidiomycete fungus with a necrotrophic lifestyle which is classified into fourteen reproductively incompatible anastomosis groups (AGs). One of these, AG8, is a devastating pathogen causing bare patch of cereals, brassicas and legumes. R. solani is a multinucleate heterokaryon containing significant heterozygosity within a single cell. This complexity posed significant challenges for the assembly of its genome. We present a high quality genome assembly of R. solani AG8 and a manually curated set of 13,964 genes supported by RNA-seq. The AG8 genome assembly used novel methods to produce a haploid representation of its heterokaryotic state. The whole-genomes of AG8, the rice pathogen AG1-IA and the potato pathogen AG3 were observed to be syntenic and co-linear. Genes and functions putatively relevant to pathogenicity were highlighted by comparing AG8 to known pathogenicity genes, orthology databases spanning 197 phytopathogenic taxa and AG1-IA. We also observed SNP-level "hypermutation" of CpG dinucleotides to TpG between AG8 nuclei, with similarities to repeat-induced point mutation (RIP). Interestingly, gene-coding regions were widely affected along with repetitive DNA, which has not been previously observed for RIP in mononuclear fungi of the Pezizomycotina. The rate of heterozygous SNP mutations within this single isolate of AG8 was observed to be higher than SNP mutation rates observed across populations of most fungal species compared. Comparative analyses were combined to predict biological processes relevant to AG8 and 308 proteins with effector-like characteristics, forming a valuable resource for further study of this pathosystem. Predicted effector-like proteins had elevated levels of non-synonymous point mutations relative to synonymous mutations (dN/dS), suggesting that they may be under diversifying selection pressures. In addition, the distant relationship to sequenced necrotrophs of the Ascomycota suggests the R. solani genome sequence may prove to be a useful resource in future comparative analysis of plant pathogens.

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Comparative Genomics Provides Insight into the Function of Broad-Host Range Sponge Symbionts.

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