Evgeny M Zdobnov

Meromictic Lake Cadagno is a permanently stratified system with a persistent microbial bloom within the oxic-anoxic boundary called the chemocline. The association between oxygenic and anoxygenic photosynthesis within the chemocline has been known for at least two decades. Although anoxygenic purple and green sulfur bacteria have been well studied, reports on oxygenic phytoplankton have remained sparse since their discovery in the 1920s. Nearly a century later, this study presents the first near-complete genome of a photosynthetic microbial eukaryote from the chemocline of Lake Cadagno, provisionally named Chlorella-like MAG. The 18.9 Mbp nuclear genome displays a high GC content (71.5%), and the phylogenetic placement suggests that it is a novel species of the genus Chlorella of Chlorophytes. Functional annotation of the Chlorella-like metagenome-assembled genome predicted 10,732 protein-coding genes, with an approximate 0.6% proportion potentially involved in carbon, sulfur, and nitrogen (C, N, and S) metabolism. In addition to C4 photosynthesis, this study detected genes for heat shock proteins (HSPs) in the Chlorella-like algae, consistent with the other Chlorella species. Altogether, the genomic insights in this study suggest the cooperation of photosynthetic algae with phototrophic sulfur bacteria via C, N, and S metabolism, which may aid their collective persistence in the Lake Cadagno chemocline. Furthermore, this work additionally presents the chloroplast genome of Cryptomonas-like species, which was likely to be presumed as cyanobacteria in previous studies because of the presence of phycobilisomes.

As a window into the past, this study offers insights into the potential role that microbial guilds may have played in the production and recycling of organic matter in ancient Proterozoic ocean chemoclines. The new observations described here suggest that chloroplasts of eukaryotic algae were persistent in the low-oxygen upper chemocline along with the purple and green sulfur bacteria known to dominate the lower half of the chemocline.