Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, SE-75123, Uppsala, Sweden.
Department of Pharmaceutical Biosciences, Biomedical Center, Uppsala University, SE-75123, Uppsala, Sweden.
ISME J. 2022 Dec;16(12):2725-2740. doi: 10.1038/s41396-022-01305-9. Epub 2022 Aug 30.
Sponge microbiomes contribute to host health, nutrition, and defense through the production of secondary metabolites. Chlamydiae, a phylum of obligate intracellular bacteria ranging from animal pathogens to endosymbionts of microbial eukaryotes, are frequently found associated with sponges. However, sponge-associated chlamydial diversity has not yet been investigated at the genomic level and host interactions thus far remain unexplored. Here, we sequenced the microbiomes of three sponge species and found high, though variable, Chlamydiae relative abundances of up to 18.7% of bacteria. Using genome-resolved metagenomics 18 high-quality sponge-associated chlamydial genomes were reconstructed, covering four chlamydial families. Among these, Candidatus Sororchlamydiaceae shares a common ancestor with Chlamydiaceae animal pathogens, suggesting long-term co-evolution with animals. Based on gene content, sponge-associated chlamydiae resemble members from the same family more than sponge-associated chlamydiae of other families, and have greater metabolic versatility than known chlamydial animal pathogens. Sponge-associated chlamydiae are also enriched in genes for degrading diverse compounds found in sponges. Unexpectedly, we identified widespread genetic potential for secondary metabolite biosynthesis across Chlamydiae, which may represent an unexplored source of novel natural products. This finding suggests that Chlamydiae members may partake in defensive symbioses and that secondary metabolites play a wider role in mediating intracellular interactions. Furthermore, sponge-associated chlamydiae relatives were found in other marine invertebrates, pointing towards wider impacts of the Chlamydiae phylum on marine ecosystems.
海绵微生物组通过次生代谢产物的产生来促进宿主的健康、营养和防御。衣原体是一类专性细胞内细菌，从动物病原体到微生物真核生物的内共生体都有，它们经常与海绵有关联。然而，海绵相关衣原体的多样性尚未在基因组水平上进行研究，宿主相互作用也尚未得到探索。在这里，我们对三种海绵物种的微生物组进行了测序，发现了高丰度但可变的衣原体，其相对丰度高达细菌的 18.7%。使用基于基因组的宏基因组学，我们重建了 18 个高质量的海绵相关衣原体基因组，涵盖了四个衣原体科。其中，候选索氏衣原体科与衣原体科动物病原体有共同的祖先，这表明它们与动物有长期的共同进化。根据基因组成，海绵相关衣原体与同一家族的成员更相似，而与其他家族的海绵相关衣原体相比，它们具有更大的代谢多样性。海绵相关衣原体也富含降解海绵中各种化合物的基因。出乎意料的是，我们在衣原体中发现了广泛的次生代谢产物生物合成的遗传潜力，这可能代表了一个未被探索的新型天然产物来源。这一发现表明，衣原体成员可能参与防御共生，次生代谢产物在调节细胞内相互作用方面发挥着更广泛的作用。此外，在其他海洋无脊椎动物中也发现了与海绵相关的衣原体亲缘关系，这表明衣原体门对海洋生态系统的影响更为广泛。
