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Anaerobic metabolism of Foraminifera thriving below the seafloor.
The ISME Journal ( IF 10.8 ) Pub Date : 2020-07-08 , DOI: 10.1038/s41396-020-0708-1
William D Orsi 1, 2 , Raphaël Morard 3 , Aurele Vuillemin 1 , Michael Eitel 1 , Gert Wörheide 1, 2, 4 , Jana Milucka 5 , Michal Kucera 3
Affiliation  

Foraminifera are single-celled eukaryotes (protists) of large ecological importance, as well as environmental and paleoenvironmental indicators and biostratigraphic tools. In addition, they are capable of surviving in anoxic marine environments where they represent a major component of the benthic community. However, the cellular adaptations of Foraminifera to the anoxic environment remain poorly constrained. We sampled an oxic-anoxic transition zone in marine sediments from the Namibian shelf, where the genera Bolivina and Stainforthia dominated the Foraminifera community, and use metatranscriptomics to characterize Foraminifera metabolism across the different geochemical conditions. Relative Foraminifera gene expression in anoxic sediment increased an order of magnitude, which was confirmed in a 10-day incubation experiment where the development of anoxia coincided with a 20–40-fold increase in the relative abundance of Foraminifera protein encoding transcripts, attributed primarily to those involved in protein synthesis, intracellular protein trafficking, and modification of the cytoskeleton. This indicated that many Foraminifera were not only surviving but thriving, under the anoxic conditions. The anaerobic energy metabolism of these active Foraminifera was characterized by fermentation of sugars and amino acids, fumarate reduction, and potentially dissimilatory nitrate reduction. Moreover, the gene expression data indicate that under anoxia Foraminifera use the phosphogen creatine phosphate as an ATP store, allowing reserves of high-energy phosphate pool to be maintained for sudden demands of increased energy during anaerobic metabolism. This was co-expressed alongside genes involved in phagocytosis and clathrin-mediated endocytosis (CME). Foraminifera may use CME to utilize dissolved organic matter as a carbon and energy source, in addition to ingestion of prey cells via phagocytosis. These anaerobic metabolic mechanisms help to explain the ecological success of Foraminifera documented in the fossil record since the Cambrian period more than 500 million years ago.



中文翻译:

海底下有孔虫的厌氧代谢。

有孔虫是具有重要生态意义的单细胞真核生物(原生生物),也是环境和古环境指标和生物地层学工具。此外,它们能够在缺氧的海洋环境中生存,它们是底栖生物群落的主要组成部分。然而,有孔虫对缺氧环境的细胞适应性仍然受到很差的限制。我们在纳米比亚大陆架的海洋沉积物中取样了一个好氧-缺氧过渡带,其中玻利维亚属Stainforthia主导有孔虫群落,并使用元转录组学来表征不同地球化学条件下的有孔虫代谢。缺氧沉积物中的相对有孔虫基因表达增加了一个数量级,这在 10 天的孵化实验中得到证实,其中缺氧的发展与有孔虫蛋白编码转录物的相对丰度增加 20-40 倍相吻合,主要归因于那些参与蛋白质合成、细胞内蛋白质运输和细胞骨架修饰的分子。这表明在缺氧条件下,许多有孔虫不仅存活而且繁衍。这些活跃的有孔虫的无氧能量代谢的特征是糖和氨基酸的发酵,富马酸盐的减少,和潜在的异化硝酸盐还原。此外,基因表达数据表明,在缺氧条件下,有孔虫使用磷原磷酸肌酸作为 ATP 储存,允许维持高能磷酸盐池的储备,以应对无氧代谢过程中突然增加的能量需求。这与参与吞噬作用和网格蛋白介导的内吞作用 (CME) 的基因一起共同表达。有孔虫除了通过吞噬作用摄取猎物细胞外,还可以使用 CME 来利用溶解的有机物作为碳和能源。这些厌氧代谢机制有助于解释自 5 亿多年前寒武纪以来化石记录中记载的有孔虫的生态成功。基因表达数据表明,在缺氧条件下,有孔虫使用磷原磷酸肌酸作为 ATP 储存器,从而可以维持高能磷酸盐池的储备,以应对无氧代谢过程中突然增加的能量需求。这与参与吞噬作用和网格蛋白介导的内吞作用 (CME) 的基因一起共同表达。有孔虫除了通过吞噬作用摄取猎物细胞外,还可以使用 CME 来利用溶解的有机物作为碳和能源。这些厌氧代谢机制有助于解释自 5 亿多年前寒武纪以来化石记录中记载的有孔虫的生态成功。基因表达数据表明,在缺氧条件下,有孔虫使用磷原磷酸肌酸作为 ATP 储存器,从而可以维持高能磷酸盐池的储备,以应对无氧代谢过程中突然增加的能量需求。这与参与吞噬作用和网格蛋白介导的内吞作用 (CME) 的基因一起共同表达。有孔虫除了通过吞噬作用摄取猎物细胞外,还可以使用 CME 来利用溶解的有机物作为碳和能源。这些厌氧代谢机制有助于解释自 5 亿多年前寒武纪以来化石记录中记载的有孔虫的生态成功。这与参与吞噬作用和网格蛋白介导的内吞作用 (CME) 的基因一起共同表达。有孔虫除了通过吞噬作用摄取猎物细胞外,还可以使用 CME 来利用溶解的有机物作为碳和能源。这些厌氧代谢机制有助于解释自 5 亿多年前寒武纪以来化石记录中记载的有孔虫的生态成功。这与参与吞噬作用和网格蛋白介导的内吞作用 (CME) 的基因一起共同表达。有孔虫除了通过吞噬作用摄取猎物细胞外,还可以使用 CME 来利用溶解的有机物作为碳和能源。这些厌氧代谢机制有助于解释自 5 亿多年前寒武纪以来化石记录中记载的有孔虫的生态成功。

更新日期:2020-07-08
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