RD3 Marine Ecology, RU Marine Symbioses, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany.
Institut de Ciències del Mar, ICM - CSIC, Barcelona, Spain.
BMC Genomics. 2024 Jul 7;25(1):674. doi: 10.1186/s12864-024-10548-z.
Sponges (phylum Porifera) constantly interact with microbes. They graze on microbes from the water column by filter-feeding and they harbor symbiotic partners within their bodies. In experimental setups, sponges take up symbionts at lower rates compared with seawater microbes. This suggests that sponges have the capacity to differentiate between microbes and preferentially graze in non-symbiotic microbes, although the underlying mechanisms of discrimination are still poorly understood. Genomic studies showed that, compared to other animal groups, sponges present an extended repertoire of immune receptors, in particular NLRs, SRCRs, and GPCRs, and a handful of experiments showed that sponges regulate the expression of these receptors upon encounter with microbial elicitors. We hypothesize that sponges may rely on differential expression of their diverse repertoire of poriferan immune receptors to sense different microbial consortia while filter-feeding. To test this, we characterized the transcriptomic response of two sponge species, Aplysina aerophoba and Dysidea avara, upon incubation with microbial consortia extracted from A. aerophoba in comparison with incubation with seawater microbes. The sponges were sampled after 1 h, 3 h, and 5 h for RNA-Seq differential gene expression analysis.
D. avara incubated with A. aerophoba-symbionts regulated the expression of genes related to immunity, ubiquitination, and signaling. Within the set of differentially-expressed immune genes we identified different families of Nucleotide Oligomerization Domain (NOD)-Like Receptors (NLRs). These results represent the first experimental evidence that different types of NLRs are involved in microbial discrimination in a sponge. In contrast, the transcriptomic response of A. aerophoba to its own symbionts involved comparatively fewer genes and lacked genes encoding for immune receptors.
Our work suggests that: (i) the transcriptomic response of sponges upon microbial exposure may imply "fine-tuning" of baseline gene expression as a result of their interaction with microbes, (ii) the differential response of sponges to microbial encounters varied between the species, probably due to species-specific characteristics or related to host's traits, and (iii) immune receptors belonging to different families of NLR-like genes played a role in the differential response to microbes, whether symbionts or food bacteria. The regulation of these receptors in sponges provides further evidence of the potential role of NLRs in invertebrate host-microbe interactions. The study of sponge responses to microbes exemplifies how investigating different animal groups broadens our knowledge of the evolution of immune specificity and symbiosis.
海绵（多孔动物门）不断与微生物相互作用。它们通过滤食从水柱中摄食微生物，并在体内栖息共生伙伴。在实验设置中，与海水微生物相比，海绵吸收共生体的速度较慢。这表明海绵有能力区分微生物，并优先在非共生微生物中摄食，尽管其背后的识别机制仍知之甚少。基因组研究表明，与其他动物群相比，海绵具有扩展的免疫受体 repertoire，特别是 NLRs、SRCRs 和 GPCRs，并且少数实验表明，海绵在遇到微生物诱导剂时会调节这些受体的表达。我们假设，海绵可能依赖于其多样化的海绵免疫受体 repertoire 的差异表达来感知滤食过程中的不同微生物群落。为了验证这一点，我们对两种海绵物种，Aplysina aerophoba 和 Dysidea avara，在与从 A. aerophoba 中提取的微生物群落孵育后，以及与海水微生物孵育后的转录组反应进行了表征。在孵育 1 小时、3 小时和 5 小时后，从 RNA-Seq 差异基因表达分析中采集海绵样本。
与 A. aerophoba 共生体孵育的 D. avara 调节了与免疫、泛素化和信号转导相关的基因表达。在差异表达的免疫基因中，我们鉴定出不同家族的核苷酸寡聚化结构域（NOD）样受体（NLRs）。这些结果代表了第一个实验证据，表明不同类型的 NLRs参与了海绵中微生物的识别。相比之下，A. aerophoba 对自身共生体的转录组反应涉及的基因相对较少，并且缺乏编码免疫受体的基因。
我们的工作表明：（i）海绵在暴露于微生物时的转录组反应可能意味着由于与微生物的相互作用，基础基因表达的“微调”，（ii）海绵对微生物接触的差异反应在物种间存在差异，可能是由于物种特异性特征或与宿主特征有关，（iii）属于不同 NLR 样基因家族的免疫受体在对微生物的差异反应中发挥作用，无论是共生体还是食物细菌。海绵中这些受体的调节为 NLRs 在无脊椎动物宿主-微生物相互作用中的潜在作用提供了进一步的证据。对海绵对微生物的反应的研究说明了研究不同动物群如何拓宽我们对免疫特异性和共生进化的认识。
