Hydrothermal plumes as hotspots for deep-ocean heterotrophic microbial biomass production

Abstract

Carbon budgets of hydrothermal plumes result from the balance between carbon sinks through plume chemoautotrophic processes and carbon release via microbial respiration. However, the lack of comprehensive analysis of the metabolic processes and biomass production rates hinders an accurate estimate of their contribution to the deep ocean carbon cycle. Here, we use a biogeochemical model to estimate the autotrophic and heterotrophic production rates of microbial communities in hydrothermal plumes and validate it with in situ data. We show how substrate limitation might prevent net chemolithoautotrophic production in hydrothermal plumes. Elevated prokaryotic heterotrophic production rates (up to 0.9 gCm^-2y^-1) compared to the surrounding seawater could lead to 0.05 GtCy^-1 of C-biomass produced through chemoorganotrophy within hydrothermal plumes, similar to the Particulate Organic Carbon (POC) export fluxes reported in the deep ocean. We conclude that hydrothermal plumes must be accounted for as significant deep sources of POC in ocean carbon budgets.

Fig. 1. Chemolithoautotrophic and chemoorganotrophic biomass production rates in hydrothermal non-buoyant plumes: model outputs and measurements.

a Chemolithoautotrophic biomass production rates from the CrabSpa vent field: comparison between NBP model outputs and fluid incubation data from ref. . b Distribution of the type of metabolisms responsible for the primary production at the CrabSpa vent field: comparison between NBP model outputs and fluid incubation data from ref. . c Chemoorganotrophic and chemolithautotrophic biomass production predicted for the El Hierro eruption based on data from ref. . d Distribution of the type of metabolisms responsible for the chemoorganotrophic and chemolithoautotrophic biomass production predicted for the El Hierro eruption based on data from ref. . e Chemoorganotrophic biomass production rates within the TAG vent non-buoyant plume: comparison between model outputs and data derived from ³H-Leucine incorporations (conventionally designed as prokaryotic heterotrophic production, PHP) rates on incubations performed during the BICOSE 2 cruise. Boxplots denote the median (center line) and interquartile range (box), with whiskers extending to three times the interquartile range and points indicating values outside this range.

Fig. 2. Global prokaryotic biomass production through chemoorganotrophic processes within non-buoyant hydrothermal plumes.

a Chemoorganotrophic production rates as a function of heat flux for various hydrothermal sites from the Mid-Atlantic Ridge (MAR: Rainbow, Tour Eiffel, Broken Spur, TAG), the East-Pacific Rise - Grand Bonum site (EPR, GB), the Main Endeavor vent field (Dante), and the Central Indian Ridge (CIR: Kairei). b Global map of the chemoorganotrophic production rates within the non-buoyant plume for the following hydrothermal sites on the MAR (Rainbow, Tour Eiffel, Logatchev, Broken Spur, TAG, Ashadze), the EPR (Grand Bonum, EPR, GB), the Main Endeavor vent Field (Dante), and the CIR (Kairei, Edmonds).