Particulate Metabolites and Transcripts Reflect Diel Oscillations of Microbial Activity in the Surface Ocean.
Particulate Metabolites and Transcripts Reflect Diel Oscillations of Microbial Activity in the Surface Ocean.
复制标题
DOI：
10.1128/msystems.00896-20
复制
发表时间：
2021-05-04
期刊：
影响因子：
6.4
通讯作者：
Ingalls AE
中科院分区：
文献类型：
--
作者：
Boysen AK;Carlson LT;Durham BP;Groussman RD;Aylward FO;Ribalet F;Heal KR;White AE;DeLong EF;Armbrust EV;Ingalls AE
在阳光照耀的海洋中，光为初级生产者的光合作用和有机物质生产提供燃料。产生的有机物的数量和质量影响群落的功能，但缺乏对细胞代谢产物--生物循环中的代谢物的现场测量。我们通过在8天内每隔4小时对15米处的颗粒状有机物中的79种代谢物进行量化，评估了北太平洋副热带环流光振荡对群落水平的生化影响。总颗粒代谢物浓度在黄昏时达到峰值，占总颗粒有机碳(POC)的2%。55/79(70%)个体代谢物的浓度具有明显的24小时周期性，日变化倍数从1.6到12.8，通常大于POC和流式细胞仪可分辨生物量的浓度，从1.2到2.8。配对的转录组分析揭示了与代谢物子集的生产和消费有关的分类群。参与合成代谢和氧化还原维持的初级代谢物具有显着的24小时周期性，不同的生物与这些代谢物相关的转录本丰度具有明显的周期性。具有渗透特性的化合物显示出最大的浓度波动，这意味着快速周转，并支持先前证据表明，功能超出了细胞膨胀维持。海藻糖与转录组和培养数据的每日大幅波动表明，海藻糖是由固氮蓝藻Crocosphaera产生的，可能为夜间新陈代谢储存能量。颗粒代谢物和转录本的配对测量共同解决了微生物用来管理日常能量和氧化还原振荡的策略，并突出了海洋微生物生态系统中具有隐秘作用的动态代谢物。在光的推动下，浮游植物产生支持海洋生态系统和碳固存的有机物。海洋变化影响微生物新陈代谢，并对生物地球化学循环产生影响。作为细胞代谢的小分子产物，代谢物往往会随着环境条件的变化而迅速变化，形成细胞内能量和营养管理和储存的基础。通过对分层表层海洋中代谢物和基因表达的配对测量，我们揭示了昼夜循环中微生物能量管理的策略，并假设振荡的代谢物是浮游植物暗呼吸的重要底物。这些对现场代谢物浓度的高分辨率Diel测量形成了未来研究这些化合物在海洋微生物群落中所扮演的具体角色的基础。
Light fuels photosynthesis and organic matter production by primary producers in the sunlit ocean. The quantity and quality of the organic matter produced influence community function, yet in situ measurements of metabolites, the products of cellular metabolism, over the diel cycle are lacking. We evaluated community-level biochemical consequences of oscillations of light in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter from 15 m every 4 h over 8 days. Total particulate metabolite concentration peaked at dusk and represented up to 2% of total particulate organic carbon (POC). The concentrations of 55/79 (70%) individual metabolites exhibited significant 24-h periodicity, with daily fold changes from 1.6 to 12.8, often greater than those of POC and flow cytometry-resolvable biomass, which ranged from 1.2 to 2.8. Paired metatranscriptome analysis revealed the taxa involved in production and consumption of a subset of metabolites. Primary metabolites involved in anabolism and redox maintenance had significant 24-h periodicity and diverse organisms exhibited diel periodicity in transcript abundance associated with these metabolites. Compounds with osmotic properties displayed the largest oscillations in concentration, implying rapid turnover and supporting prior evidence of functions beyond cell turgor maintenance. The large daily oscillation of trehalose paired with metatranscriptome and culture data showed that trehalose is produced by the nitrogen-fixing cyanobacterium Crocosphaera, likely to store energy for nighttime metabolism. Together, paired measurements of particulate metabolites and transcripts resolve strategies that microbes use to manage daily energy and redox oscillations and highlight dynamic metabolites with cryptic roles in marine microbial ecosystems. IMPORTANCE Fueled by light, phytoplankton produce the organic matter that supports ocean ecosystems and carbon sequestration. Ocean change impacts microbial metabolism with repercussions for biogeochemical cycling. As the small molecule products of cellular metabolism, metabolites often change rapidly in response to environmental conditions and form the basis of energy and nutrient management and storage within cells. By pairing measurements of metabolites and gene expression in the stratified surface ocean, we reveal strategies of microbial energy management over the day-night cycle and hypothesize that oscillating metabolites are important substrates for dark respiration by phytoplankton. These high-resolution diel measurements of in situ metabolite concentrations form the basis for future work into the specific roles these compounds play in marine microbial communities.