Nilsen Tonje, Pettersen Ragnhild, Keeley Nigel Brian, Ray Jessica Louise, Majaneva Sanna, Stokkan Morten, Hervik Anja, Angell Inga Leena, Snipen Lars Gustav, Sundt Maud Ødegaard, Rudi Knut
Norwegian University of Life Sciences, Ås 1433, Norway.
Akvaplan-niva, Tromsø 9007, Norway.
Environ Sci Technol. 2025 Apr 22;59(15):7517-7529. doi: 10.1021/acs.est.4c12464. Epub 2025 Apr 11.
Recent evidence suggests that there is a major switch in coastal seafloor microbial ecology already at a mildly deteriorated macrofaunal state. This knowledge is of critical value in the management and conservation of the coastal seafloor. We therefore aimed to determine the relationships between seafloor microbiota and macrofauna on a regional scale. We compared prokaryote, macrofauna, chemical, and geographical data from 1546 seafloor samples, which varied in their exposure to aquaculture activities along the Norwegian and Icelandic coasts. We found that the seafloor samples contained either a network centralized by a sulfur oxidizer (42.4% of samples, = 656) or a network centralized by an archaeal ammonium oxidizer (44.0% of samples, = 681). Very few samples contained neither network (9.8% of samples, = 151) or both (3.8% of samples, = 58). Samples with a sulfur oxidizer network had a 10-fold higher risk of macrofauna loss (odds ratios, 95% CI: 9.5 to 15.6), while those with an ammonium oxidizer network had a 10-fold lower risk (95% CI: 0.068 to 0.11). The sulfur oxidizer network was negatively correlated to distance from Norwegian aquaculture sites (Spearman rho = -0.42, < 0.01) and was present in all Icelandic samples ( = 274). The ammonium oxidizer network was absent from Icelandic samples and positively correlated to distance from Norwegian aquaculture sites (Spearman rho = 0.67, < 0.01). Based on 356 high-quality metagenome-assembled genomes (MAGs), we found that bicarbonate-dependent carbon fixation and low-affinity oxygen respiration were associated with the ammonium oxidizer network, while the sulfur oxidizer network was associated with ammonium retention, sulfur metabolism, and high-affinity oxygen respiration. In conclusion, our findings highlight the critical roles of microbial networks centralized by sulfur and ammonium oxidizers in mild macrofauna deterioration, which should be included as an essential part of seafloor surveillance.
近期证据表明，在大型底栖动物状态轻度恶化时，沿海海底微生物生态就已发生重大转变。这一认知在沿海海底的管理和保护中具有至关重要的价值。因此，我们旨在确定区域尺度上海底微生物群与大型底栖动物之间的关系。我们比较了来自1546个海底样本的原核生物、大型底栖动物、化学和地理数据，这些样本在挪威和冰岛海岸沿线受水产养殖活动的影响程度各不相同。我们发现，海底样本要么包含一个以硫氧化菌为中心的网络（占样本的42.4%，n = 656），要么包含一个以古菌氨氧化菌为中心的网络（占样本的44.0%，n = 681）。极少样本既不包含这两个网络（占样本的9.8%，n = 151），也不包含两个网络（占样本的3.8%，n = 58）。拥有硫氧化菌网络的样本大型底栖动物损失风险高出10倍（优势比，95%置信区间：9.5至15.6），而拥有氨氧化菌网络的样本风险则低10倍（95%置信区间：0.068至0.11）。硫氧化菌网络与距挪威水产养殖场所的距离呈负相关（斯皮尔曼等级相关系数rho = -0.42，P < 0.01），且在所有冰岛样本（n = 274）中均存在。冰岛样本中不存在氨氧化菌网络，且其与距挪威水产养殖场所的距离呈正相关（斯皮尔曼等级相关系数rho = 0.67，P < 0.01）。基于356个高质量的宏基因组组装基因组（MAG），我们发现依赖碳酸氢盐的碳固定和低亲和力氧呼吸与氨氧化菌网络相关，而硫氧化菌网络与氨保留、硫代谢和高亲和力氧呼吸相关。总之，我们的研究结果凸显了以硫和氨氧化菌为中心的微生物网络在大型底栖动物轻度退化中的关键作用，应将其纳入海底监测的重要组成部分。
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