Clara Priemer

More than 200 years ago, Alexander von Humboldt described a tree of the genus Clusia for its ability to perform crassulacean acid metabolism (CAM). This drought-adaptive metabolism allows plants to maintain photosynthesis under water limitation by temporally separating CO₂ uptake and fixation. The diversity of CAM physiotypes has fueled a debate about evolutionary constraints and the feasibility of engineering CAM into C₃ crops. The genus Clusia displays an exceptional diversity of photosynthetic physiotypes, yet genome sequences and genomic mechanisms generating this diversity remain unresolved. Here, we sequence and compare the genomes of three Clusia species spanning weak, inducible, and strong CAM. We show that polyploidization followed by transposon-mediated genic diploidization could have shaped CAM-related gene families, particularly those controlling phosphoenol-pyruvate recycling via phosphorolytic leaf starch metabolism. Our results indicate that whole-genome duplication coupled to diploidization might have driven diversification of CAM physiotypes in Clusia , providing a genomic framework for understanding CAM diversity and evolution.

Sulfoquinovose, a sulfonated sugar derived from the thylakoid membrane lipid sulfoquinovosyl diacylglycerol, is abundant in photosynthetic organisms and plays a key role in global sulfur cycling. Its degradation in nature is mediated by specialized bacteria, many of which rely on the enzyme sulfoquinovosidase (YihQ) to release sulfoquinovose from sulfoquinovosyl (diacyl)glycerol. Despite its ecological importance, the diversity and functional roles of sulfoquinovose-degrading microorganisms remain poorly characterized in natural environments. Here, we developed a yihQ-targeted amplicon sequencing approach to investigate the richness and distribution of SQ-degrading bacteria across selected environments. We revealed high richness of yihQ-containing microorganisms in the analyzed cow rumen samples, far exceeding that observed in human and mouse gut microbiomes, suggesting an important role of sulfoquinovose metabolism in ruminant digestion. Anoxic microcosm experiments with sulfoquinovose-amended rumen fluid revealed cooperative microbial degradation of sulfoquinovose to sulfide via isethionate cross-feeding. Amplicon sequencing and genome-resolved metagenomics and metatranscriptomics identified yet undescribed and uncultured sulfoquinovose-degrading taxa. Members of Caproiciproducens (Acutalibacteraceae), Candidatus Limivicinus (Oscillospiraceae), and Sphaerochaetaceae transcribed the isethionate-producing sulfo-transketolase pathway, whereas isethionate was likely respired by a Candidatus Mailhella bacterium (Desulfovibrionaceae). This study presents a functional gene-based assay for tracking environmental yihQ richness, highlights sulfoquinovose degradation as a central metabolic process in the cow rumen, describes previously unknown sulfoquinovose-metabolizing bacteria, and advances understanding of sulfur physiology in complex microbial communities.

The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterized by the repeated evolution of Crassulacean acid metabolism (CAM). Despite its complex genetic basis, this water-conserving trait has evolved independently across many plant families and is regarded as a key innovation trait and driver of ecological diversification in Bromeliaceae. By producing high-quality genome assemblies of a Tillandsia species pair displaying divergent photosynthetic phenotypes, and combining genome-wide investigations of synteny, transposable element (TE) dynamics, sequence evolution, gene family evolution, and temporal differential expression, we were able to pinpoint the genomic drivers of CAM evolution in Tillandsia. Several large-scale rearrangements associated with karyotype changes between the 2 genomes and a highly dynamic TE landscape shaped the genomes of Tillandsia. However, our analyses show that rewiring of photosynthetic metabolism is mainly obtained through regulatory evolution rather than coding sequence evolution, as CAM-related genes are differentially expressed across a 24-h cycle between the 2 species but are not candidates of positive selection. Gene orthology analyses reveal that CAM-related gene families manifesting differential expression underwent accelerated gene family expansion in the constitutive CAM species, further supporting the view of gene family evolution as a driver of CAM evolution.