Metapangenomics reveals depth-dependent shifts in metabolic potential for the ubiquitous marine bacterial SAR324 lineage

BackgroundOceanic microbiomes play a pivotal role in the global carbon cycle and are central to the transformation and recycling of carbon and energy in the ocean’s interior. SAR324 is a ubiquitous but poorly understood uncultivated clade of Deltaproteobacteria that inhabits the entire water column, from ocean surface waters to its deep interior. Although some progress has been made in elucidating potential metabolic traits of SAR324 in the dark ocean, very little is known about the ecology and the metabolic capabilities of this group in the euphotic and twilight zones. To investigate the comparative genomics, ecology and physiological potential of the SAR324 clade, we examined the distribution and variability of key genomic features and metabolic pathways in this group from surface waters to the abyss in the North Pacific Subtropical Gyre, one of the largest biomes on Earth.Results We leveraged a pangenomic ecological approach, combining spatio-temporally resolved single amplified genome, metagenomic and metatranscriptomic datasets. The data revealed substantial genomic diversity throughout the SAR324 clade, with distinct depth and temporal distributions that clearly differentiated ecotypes. Phylogenomic subclade delineation, environmental distributions, genomic feature similarities, and metabolic capacities revealed congruent groups that, when merged, form Operational Ecogenomic Units (OEUs). The four SAR324 OEUs delineated in this study revealed striking divergence from one another with respect to their habitat-specific metabolic potentials. The OEUs living in the dark or twilight oceans shared genomic features and metabolic capabilities consistent with a sulfur-based chemolithoautotrophic lifestyle. In contrast, those inhabiting the sunlit ocean displayed higher plasticity energy-related metabolic pathways, supporting a presumptive photoheterotrophic lifestyle. In epipelagic SAR324 OEUs, we observed the presence of two types of proton-pumping rhodopsins, as well as genomic, transcriptomic, and ecological evidence for active photoheterotrophy, based on xanthorhodopsin-like light-harvesting proteins.ConclusionsOur approach combining pangenomic and multi-omics profiling revealed a striking divergence in the vertical distribution, genomic composition, metabolic potential, and predicted lifestyle strategies of geographically co-located members of the SAR324 bacterial clade. The results highlight the utility of pangenomic approaches employed across environmental gradients, to decipher the properties and variation in function and ecological traits of specific phylogenetic clades within complex microbiomes.