Abstract
To decipher the response of mesopelagic prokaryotic communities to input of nutrients, we tracked changes in prokaryotic abundance, extracellular enzymatic activities, heterotrophic production, dark dissolved inorganic carbon (DIC) fixation, community composition (16S rRNA sequencing) and community gene expression (metatranscriptomics) in 3 microcosm experiments with water from the mesopelagic North Atlantic. Responses in 3 different treatments amended with thiosulfate, ammonium or organic matter (i.e., pyruvate plus acetate) were compared to unamended controls. The strongest stimulation was found in the organic matter enrichments, where all measured rates increased >10-fold. Strikingly, in the organic matter treatment, the dark DIC fixation rates—assumed to be related to autotrophic metabolisms—were equally stimulated as all the other heterotrophic-related parameters. This increase in DIC fixation rates was paralleled by an up-regulation of genes involved in DIC assimilation via anaplerotic pathways. Alkaline phosphatase was the metabolic rate most strongly stimulated and its activity seemed to be related to cross-activation by nonpartner histidine kinases, and/or the activation of genes involved in the regulation of elemental balance during catabolic processes. These findings suggest that episodic events such as strong sedimentation of organic matter into the mesopelagic might trigger rapid increases of originally rare members of the prokaryotic community, enhancing heterotrophic and autotrophic carbon uptake rates, ultimately affecting carbon cycling. Our experiments highlight a number of fairly unstudied microbial processes of potential importance in mesopelagic waters that require future attention.
Highlights
Mesopelagic heterotrophic prokaryotes rely on the organic matter generated by primary production in the sun-lit surface waters
High dark dissolved inorganic carbon (DIC) fixation rates attributed to heterotrophic bacteria have been found in surface waters (Li and Dickie, 1991; Prakash et al, 1991; Li et al, 1993; Markager, 1998; Alonso-Sáez et al, 2010), and an active DIC-fixing prokaryotic community has been observed in the mesopelagic layer of the Atlantic (Herndl et al, 2005; Reinthaler et al, 2010; Baltar et al, 2010b)
Our results indicate that the metabolic activity of the prokaryotic community of the mesopelagic subtropical North Atlantic is not stimulated by thiosulfate, but by amendments with ammonium and organic carbon
Summary
Mesopelagic heterotrophic prokaryotes rely on the organic matter generated by primary production in the sun-lit surface waters. High dark DIC fixation rates attributed to heterotrophic bacteria have been found in surface waters (Li and Dickie, 1991; Prakash et al, 1991; Li et al, 1993; Markager, 1998; Alonso-Sáez et al, 2010), and an active DIC-fixing prokaryotic community has been observed in the mesopelagic layer of the Atlantic (Herndl et al, 2005; Reinthaler et al, 2010; Baltar et al, 2010b). DIC fixation in the mesopelagic realm has been suggested as a process that could explain this imbalance between the heterotrophic carbon demand and its supply (Baltar et al, 2010b), but the energy source to sustain this DIC fixation remains enigmatic. DIC fixation potentially plays a previously unrecognized role in the mesopelagic carbon cycle, a mechanistic understanding of this process in the vast mesopelagic realm remains to be deciphered (Swan et al, 2011; Herndl and Reinthaler, 2013)
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