Molecular and Physiological Acclimation to Low Light and Iron Scarcity in Globally Abundant Oceanic Pelagophyte

Pelagomonas calceolata is a widely distributed marine alga and is among the most numerous eukaryotes on Earth. It is abundant in subsurface chlorophyll maximum layer (SCML) communities where it can be responsible for a majority of nitrate assimilation. Growth in these communities is frequently limited by the lack of iron (Fe), and no eukaryotic phytoplankton species has been shown to require less Fe than P. calceolata. SCML communities are also light limited, resulting in an increased need for Fe-rich photosynthetic proteins. Consequently, to survive and compete in these SCML environments calls for an Fe/light co-limitation specialist. To understand the strategies behind P. calceolata’s success, we profiled this organism’s physiology and gene expression as it experiences Fe/light co-limitation. Our study describes the cellular changes under steady-state Fe limitation and the short-term responses to Fe resupply. Our culture experiments revealed that P. calceolata maintains exceptionally low Fe:C ratios across conditions and dynamically regulates iron-sparing strategies such as flavodoxin expression and substitution of metal-rich proteins. Furthermore, coupling environmental gene expression with culture-based profiles showed that Fe- and light-responsive genes identified in the lab were strongly enriched in SCML metatranscriptomes, indicating that P. calceolata expresses these adaptations in situ. These results demonstrate low Fe tolerance as a key adaptation enabling P. calceolata to thrive in light-limited marine environments and highlight its broader role in oceanic carbon and nitrogen cycling.

钙囊远洋藻（Pelagomonas calceolata）是一种分布广泛的海洋藻类，也是地球上数量最为丰富的真核生物之一。该物种在次表层叶绿素最大值层（subsurface chlorophyll maximum layer, SCML）群落中数量颇丰，可承担该环境中大部分的硝酸盐同化作用。这类群落中的生物生长通常受铁（Fe）限制，且目前尚未发现有哪种真核浮游植物（eukaryotic phytoplankton）的铁需求量低于钙囊远洋藻。次表层叶绿素最大值层群落同时还受光照限制，这使得生物对富铁光合蛋白的需求进一步提升。因此，要在这类次表层叶绿素最大值层环境中存活并竞争，生物需要成为铁/光照共同限制条件下的特化物种。为了阐明钙囊远洋藻得以成功繁衍的背后策略，我们在铁/光照共同限制的条件下，对该物种的生理特性与基因表达进行了表征分析。本研究描述了稳态铁限制条件下的细胞变化，以及该物种对铁补充的短期响应。我们的培养实验结果显示，钙囊远洋藻在各类培养条件下均维持着极低的铁碳比，并能动态调控省铁策略（iron-sparing strategies），例如表达黄素氧还蛋白（flavodoxin）以及替换富金属蛋白。此外，将环境基因表达数据与培养实验得到的表达谱进行关联分析后发现，实验室中鉴定出的铁响应与光照响应基因在次表层叶绿素最大值层宏转录组（metatranscriptomes）中显著富集，这表明钙囊远洋藻在原位环境中确实表达了这些适应性机制。上述结果证实，低铁耐受性是钙囊远洋藻得以在光照受限的海洋环境中繁盛生长的关键适应性机制，同时也凸显了该物种在海洋碳氮循环中发挥的更为广泛的作用。