Adverse Environmental Perturbations May Threaten Kelp Farming Sustainability by Exacerbating Enterobacterales Diseases

Globally kelp farming is gaining attention to mitigate land-use pressures and achieve carbon neutrality. However, the influence of environmental perturbations on kelp farming remains largely unknown. Recently, a severe disease outbreak caused extensive kelp mortality in Sanggou Bay, China, one of the world’s largest high-density kelp farming areas. Here, through in situ investigations and simulation experiments, we find indications that an anomalously dramatic increase in elevated coastal seawater light penetration may have contributed to dysbiosis in the kelp Saccharina japonica’s microbiome. This dysbiosis promoted the proliferation of opportunistic pathogenic Enterobacterales, mainly including the genera Colwellia and Pseudoalteromonas. Using transcriptomic analyses, we revealed that high-light conditions likely induced oxidative stress in kelp, potentially facilitating opportunistic bacterial Enterobacterales attack that activates a terrestrial plant-like pattern recognition receptor system in kelp. Furthermore, we uncover crucial genotypic determinants of Enterobacterales dominance and pathogenicity within kelp tissue, including pathogen-associated molecular patterns, potential membrane-damaging toxins, and alginate and mannitol lysis capability. Finally, through analysis of kelp-associated microbiome data sets under the influence of ocean warming and acidification, we conclude that such Enterobacterales favoring microbiome shifts are likely to become more prevalent in future environmental conditions. Our study highlights the need for understanding complex environmental influences on kelp health and associated microbiomes for the sustainable development of seaweed farming.

全球海带养殖正日益受到关注，以期缓解土地利用压力并达成碳中和目标。然而，环境扰动对海带养殖的影响迄今仍鲜为人知。近日，中国桑沟湾——全球最大的高密度海带养殖区域之一——爆发严重病害，造成大规模海带死亡。本研究通过原位调查与模拟实验，发现沿岸海水光照穿透率异常显著升高，可能导致海带（Saccharina japonica）的微生物组发生菌群失调。该菌群失调促进了机会致病肠杆菌目（Enterobacterales）的增殖，其主要类群为科尔氏菌属（Colwellia）与假交替单胞菌属（Pseudoalteromonas）。通过转录组分析，我们发现高光条件可能诱导海带产生氧化应激，进而可能促进机会致病肠杆菌目细菌的侵染——该侵染会激活海带内类陆生植物的模式识别受体系统。此外，我们还揭示了海带组织内肠杆菌目菌群优势度与致病性的关键基因型决定因子，包括病原相关分子模式、潜在膜损伤毒素，以及褐藻胶与甘露醇裂解能力。最后，通过分析海洋变暖与酸化影响下的海带共生微生物组数据集，我们得出结论：这类偏好驱动微生物组偏移的肠杆菌目菌群，在未来环境条件下或将愈发普遍。本研究强调，为实现海藻养殖的可持续发展，亟需厘清复杂环境因素对海带健康及其共生微生物组的影响。