Biogeographic patterns and metabolic potential of chemoautotrophic communities in cold seep sediments across subarctic to tropical regions.
Cold seeps are hotspots of chemoautotrophic primary production, yet how chemoautotrophic community structure and dark carbon fixation (DCF) vary across climatic regions remains unclear. We combined incubation experiments and metagenomics to compare chemoautotrophic communities in cold seep sediments across northwestern Pacific marginal seas, from the subarctic Okhotsk Sea to the tropical South China Sea. Incubation experiments demonstrated higher DCF rates in tropical (1.20 μg C g-1 day-1) than subarctic (0.35 μg C g-1 day-1) sediments (p = 0.002). Analyses of 133 cold seep sediment metagenomes (26 in this study and 107 from NCBI, spanning 0-240 cmbsf) revealed that subarctic chemoautotrophs were dominated by Chloroflexota, Asgardarchaeota, Campylobacterota, and Thermoproteota, whereas tropical chemoautotrophs were dominated by Pseudomonadota and Asgardarchaeota, with higher alpha diversity and integrated co-occurrence networks observed in tropical sediments. Representative genes of the Calvin-Benson-Bassham (CBB) cycle, the 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) cycle, and the 3-hydroxypropionate (3HP) bicycle were enriched in tropical sediments, whereas reductive tricarboxylic acid (rTCA) cycle and Wood-Ljungdahl (WL) pathway genes predominated in subarctic sediments. Genome-resolved analysis showed that CBB cycle potential was concentrated in Pseudomonadota in tropical sediments and in Asgardarchaeota in subarctic sediments, and was most strongly correlated with nitrogen metabolism genes, whereas rTCA cycle potential was concentrated in Campylobacterota across both sediments, coupled strongly to sulfur metabolism. Depth profiling revealed surface communities dominated by Campylobacteria using rTCA cycle in subarctic sediments, and Alphaproteobacteria and Gammaproteobacteria using CBB cycle in tropical sediments, whereas the WL pathway predominated in Dehalococcoidia and Lokiarchaeia in the deeper layers of both regions. This study provides a comparative framework for chemoautotrophic biogeography across climatically distinct seeps.