Maritan Andrew J, Clements Cody S, Pratte Zoe A, Hay Mark E, Stewart Frank J
Department of Microbiology & Cell Biology, Montana State University, Bozeman, MT 59717, United States.
School of Biological Sciences and Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, GA 30332, United States.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf088.
Sea cucumbers have been overharvested world-wide, making assessments of their ecological effects challenging, but recent research demonstrated that sea cucumbers increased coral survival via disease suppression and were therefore important for facilitating reef health. The mechanisms underpinning the sea cucumber-coral interaction are not well understood but are likely mediated through sea cucumber grazing of microbes from reef sediments. We explored how sea cucumber grazing alters the sediment microbiome by leveraging a healthy sea cucumber population on a reef in French Polynesia. We used quantitative PCR, 16S rRNA gene sequencing, and shotgun metagenomics to compare the sediment microbiome in cages placed in situ with or without sea cucumbers. We hypothesized that grazing would lower microbial biomass, change sediment microbiome composition, and deplete sediment metagenomes of anaerobic metabolisms, likely due to aeration of the sediments. Sea cucumber grazing resulted in a 75% reduction in 16S rRNA gene abundances and reshaped microbiome composition, causing a significant decrease of cyanobacteria and other phototrophs relative to ungrazed sediments. Grazing also resulted in a depletion of genes associated with cyanotoxin synthesis, suggesting a potential link to coral health. In contrast to expectations, grazed sediment metagenomes were enriched with marker genes of diverse anaerobic or microaerophilic metabolisms, including those encoding high oxygen affinity cytochrome oxidases. This enrichment differs from patterns linked to other bioturbating invertebrates. We hypothesize that grazing enriches anaerobic processes in sediment microbiomes through removal of oxygen-producing autotrophs, fecal deposition of sea cucumber gut-associated anaerobes, or modification of sediment diffusibility. These results suggest that sea cucumber harvesting influences biogeochemical processes in reef sediments, potentially mediating coral survival by altering the sediment microbiome and its production of coral-influencing metabolites.
海参在全球范围内被过度捕捞，这使得评估它们的生态影响具有挑战性，但最近的研究表明，海参通过抑制疾病提高了珊瑚的存活率，因此对促进珊瑚礁健康很重要。海参与珊瑚相互作用的机制尚未完全了解，但可能是通过海参对珊瑚礁沉积物中微生物的摄食来介导的。我们利用法属波利尼西亚一个珊瑚礁上健康的海参种群，探索了海参摄食如何改变沉积物微生物组。我们使用定量PCR、16S rRNA基因测序和鸟枪法宏基因组学，比较了原位放置有或没有海参的笼子里的沉积物微生物组。我们假设，摄食会降低微生物生物量，改变沉积物微生物组组成，并耗尽沉积物宏基因组中的厌氧代谢，这可能是由于沉积物的曝气作用。海参摄食导致16S rRNA基因丰度降低了75%，并重塑了微生物组组成，导致与未被摄食的沉积物相比，蓝细菌和其他光合生物显著减少。摄食还导致与蓝藻毒素合成相关的基因减少，这表明与珊瑚健康可能存在联系。与预期相反，被摄食的沉积物宏基因组富含各种厌氧或微需氧代谢的标记基因，包括那些编码高氧亲和力细胞色素氧化酶的基因。这种富集不同于与其他生物扰动无脊椎动物相关的模式。我们假设，摄食通过去除产氧自养生物、海参肠道相关厌氧菌的粪便沉积或沉积物扩散性的改变，丰富了沉积物微生物组中的厌氧过程。这些结果表明，海参捕捞会影响珊瑚礁沉积物中的生物地球化学过程，可能通过改变沉积物微生物组及其对珊瑚有影响的代谢产物的产生来介导珊瑚的存活。
