Growth on ATP Elicits a P-Stress Response in the Picoeukaryote Micromonas pusilla

The surface waters of oligotrophic oceans have chronically low phosphate (Pi) concentrations, which renders dissolved organic phosphorus (DOP) an important nutrient source. In the subtropical North Atlantic, cyanobacteria are often numerically dominant, but picoeukaryotes can dominate autotrophic biomass and productivity making them important contributors to the ocean carbon cycle. Despite their importance, little is known regarding the metabolic response of picoeukaryotes to changes in phosphorus (P) source and availability. To understand the molecular mechanisms that regulate P utilization in oligotrophic environments, we evaluated transcriptomes of the picoeukaryote Micromonas pusilla grown under Pi-replete and -deficient conditions, with an additional investigation of growth on DOP in replete conditions. Genes that function in sulfolipid substitution and Pi uptake increased in expression with Pi-deficiency, suggesting cells were reallocating cellular P and increasing P acquisition capabilities. Pi-deficient M. pusilla cells also increased alkaline phosphatase activity and reduced their cellular P content. Cells grown with DOP were able to maintain relatively high growth rates, however the transcriptomic response was more similar to the Pi-deficient response than that seen in cells grown under Pi-replete conditions. The results demonstrate that not all P sources are the same for growth; while M. pusilla, a model picoeukaryote, may grow well on DOP, the metabolic demand is greater than growth on Pi. These findings provide insight into the cellular strategies which may be used to support growth in a stratified future ocean predicted to favor picoeukaryotes.

寡营养海洋的表层水体长期处于磷酸盐（Pi）浓度极低的状态，这使得溶解态有机磷（DOP）成为重要的营养源。在亚热带北大西洋海域，蓝细菌通常在数量上占据优势，但超微型真核浮游生物（picoeukaryotes）却可主导自养生物量与生产力，因此它们是海洋碳循环的重要贡献者。尽管这类生物具有重要生态意义，但学界对超微型真核浮游生物响应磷（P）源与磷有效性变化的代谢机制仍知之甚少。为阐明寡营养环境中磷利用调控的分子机制，我们对在磷酸盐充足与缺乏条件下培养的超微型真核浮游生物代表种——微单胞藻（Micromonas pusilla）的转录组进行了分析，并额外探究了其在充足磷条件下以DOP为磷源时的生长情况。在磷酸盐缺乏条件下，参与硫脂替代与磷酸盐摄取的基因表达量显著上调，这表明细胞会重新分配胞内磷资源并提升磷获取能力。磷酸盐缺乏的微单胞藻同时还会增强碱性磷酸酶活性，并降低胞内磷含量。以DOP为磷源培养的细胞可维持相对较高的生长速率，但其转录组响应与磷酸盐缺乏组的相似性，远高于磷酸盐充足组。研究结果表明，并非所有磷源都适用于该物种的生长：作为超微型真核浮游生物的模式物种，微单胞藻虽可在DOP培养基中良好生长，但其代谢消耗要高于以Pi为磷源的情况。本研究揭示了在未来分层海洋环境中（该环境被预测更有利于超微型真核浮游生物生存），细胞可能采用的生长支持策略。