Animal burrowing at cold seep ecotones boosts productivity by linking macromolecule turnover with chemosynthesis and nutrient cycling

Abstract

Hydrocarbon seepage at the deep seafloor fuels flourishing chemosynthetic communities. These seeps impact the functionality of the benthic ecosystem beyond hotspots of gas emission, altering the abundance, diversity, and activity of microbiota and fauna and affecting geochemical processes. However, these chemosynthetic ecotones (chemotones) are far less explored than the foci of seepage. To better understand the functionality of chemotones, we (i) mapped seabed morphology at the periphery of gas seeps in the deep eastern Mediterranean Sea, using video analyses and synthetic aperture sonar; (ii) sampled chemotone sediments and described burrowing using computerized tomography; (iii) explored nutrient concentrations; (iv) quantified microbial abundance, activity, and N2 fixation rates in selected samples; and (v) extracted DNA and explored microbial diversity and function using amplicon sequencing and metagenomics. Our results show that gas seepage creates burrowing intensity gradients at seep ecotones, with the ghost shrimp Calliax lobata primarily responsible for burrowing, which influences nitrogen and sulfur cycling through microbial activity. Burrow walls form a unique habitat, where macromolecules are degraded by Bacteroidota, and their fermentation products fuel sulfate reduction by Desulfobacterota and Nitrospirota. These, in turn, support chemosynthetic Campylobacterota and giant sulfur bacteria Thiomargarita, which can aid C. lobata nutrition. These interactions may support enhanced productivity at seep ecotones.