Institute of General Microbiology, Kiel University, Kiel 24118, Germany.
GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel 24148, Germany.
Proc Natl Acad Sci U S A. 2022 Jun 21;119(25):e2200198119. doi: 10.1073/pnas.2200198119. Epub 2022 Jun 15.
Benthic foraminifera are unicellular eukaryotes that inhabit sediments of aquatic environments. Several foraminifera of the order Rotaliida are known to store and use nitrate for denitrification, a unique energy metabolism among eukaryotes. The rotaliid spp. has been shown to encode an incomplete denitrification pathway of bacterial origin. However, the prevalence of denitrification genes in foraminifera remains unknown, and the missing denitrification pathway components are elusive. Analyzing transcriptomes and metagenomes of 10 foraminiferal species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer the last common ancestor of denitrifying foraminifera, which enables us to predict the ability to denitrify for additional foraminiferal species. Additionally, an examination of the foraminiferal microbiota reveals evidence for a stable interaction with Desulfobacteraceae, which harbor genes that complement the foraminiferal denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera-associated microbiome. The interaction of foraminifera with their resident bacteria is at the basis of foraminiferal adaptation to anaerobic environments that manifested in ecological success in oxygen depleted habitats.
底栖有孔虫是一类居住在水生环境沉积物中的单细胞真核生物。已知几个旋扭虫目（Rotaliida）的有孔虫能够储存和利用硝酸盐进行反硝化作用，这是真核生物中独特的能量代谢方式。已证明旋扭虫目 spp. 编码了源自细菌的不完全反硝化途径。然而，有孔虫中反硝化基因的普遍性仍然未知，而且缺失的反硝化途径成分也难以捉摸。通过分析来自秘鲁缺氧区的 10 种有孔虫的转录组和宏基因组，我们表明反硝化基因在有孔虫中高度保守。我们推断了具有反硝化能力的有孔虫的最后共同祖先，这使我们能够预测其他有孔虫物种的反硝化能力。此外，对有孔虫微生物组的研究表明，有孔虫与脱硫杆菌科（Desulfobacteraceae）之间存在稳定的相互作用的证据，后者拥有能够补充有孔虫反硝化途径的基因。我们的研究结果提供了证据表明，有孔虫的反硝化作用是由与有孔虫相关的微生物组补充的。有孔虫与其栖息细菌的相互作用是有孔虫适应缺氧环境的基础，这种适应在缺氧栖息地的生态成功中得到了体现。
