Heterotrophic bicarbonate assimilation is the main process of de novo organic carbon synthesis in hadal zone of the Hellenic Trench, the deepest part of Mediterranean Sea

Abstract

Ammonium-oxidizing chemoautotrophic members of Thaumarchaea are proposed to be the key players in the assimilation of bicarbonate in the dark (ABD). However, this process may also involve heterotrophic metabolic pathways, such as fixation of carbon dioxide (CO2) via various anaplerotic reactions. We collected samples from the depth of 4900 m at the Matapan-Vavilov Deep (MVD) station (Hellenic Trench, Eastern Mediterranean) and used the multiphasic approach to study the ABD mediators in this deep-sea ecosystem. At this depth, our analysis indicated the occurrence of actively CO2-fixing heterotrophic microbial assemblages dominated by Gammaproteobacteria with virtually no Thaumarchaea present. [14C]-bicarbonate incorporation experiments combined with shotgun [14C]-proteomic analysis identified a series of proteins of gammaproteobacterial origin. More than quarter of them were closely related with Alteromonas macleodii ‘deep ecotype’ AltDE, the predominant organism in the microbial community of MVD. The present study demonstrated that in the aphotic/hadal zone of the Mediterranean Sea, the assimilation of bicarbonate is associated with both chemolithoauto- and heterotrophic ABD. In some deep-sea areas, the latter may predominantly contribute to the de novo synthesis of organic carbon which points at the important and yet underestimated role heterotrophic bacterial populations can play the in global carbon cycle/sink in the ocean interior.

Uptake‐release dynamics of the inorganic and organic carbon pool mediated by planktonic prokaryotes in the deep Mediterranean Sea

“…Taylor et al ., ; Manganelli et al ., ; Reinthaler et al ., ), thus being highly comparable to organoheterotrophic production rates. It has also been calculated that the amount of inorganic carbon fixed in the dark portion of the water column is in the same range of the one utilized by phototrophic microorganisms in the epipelagic zone (Yakimov et al ., ), thus strengthening the idea of the global ocean as a previously‐underestimated sink of CO 2 .…”

“…Furthermore, in the last decade, a growing amount of data have shown that inorganic carbon fixation in the dark ocean via chemosynthetic processes (Herndl et al ., ) and anaplerotic reactions (Yakimov et al ., ) occurs at measurable rates. Chemosynthesis is mainly performed by ammonia‐oxidizing members of the phylum Thaumarchaeota although several metabolic pathways (e.g.…”

“…Conversely, the uptake of CO 2 to be utilized in anaplerotic reactions is a functional trait typical of heterotrophic pathways. Most heterotrophic prokaryotes, in fact, can utilize carbon dioxide for a variety of carboxylation reactions, still depending upon OC sources for energy and C requirements (Yakimov et al ., and references therein). Dissolved inorganic carbon (DIC) uptake in the dark has been measured in several areas of the global ocean and researches pinpoint that production rates are in the order of few (up to hundreds of) ngC l −1 d −1 in meso‐ and bathypelagic systems (e.g.…”

Relative Importance of Chemoautotrophy for Primary Production in a Light Exposed Marine Shallow Hydrothermal System

“…However, our incubations were performed for a maximum of 48 h and previous studies have shown that incubation times shorter than one to 2 weeks seem to prevent labeling of heterotrophic organisms due to cross-feeding (Knief et al, 2003). Therefore, our experiments are likely to have primarily targeted autotrophic microorganisms, but co-assimilation of CO 2 by autotrophs and active members of the heterotrophic community, including thermo- or mesophilic Chloroflexi , cannot be fully excluded (e.g., Roslev et al, 2004; Yamada et al, 2006; Wegener et al, 2012; Yakimov et al, 2014; Schubotz et al, 2015). …”

Variations in Microbial Community Structure through the Stratified Water Column in the Tyrrhenian Sea (Central Mediterranean)

“…Samples were filtered through sterile 0.2-μm cellulose acetate membrane filters (SM 16534 K, Sartorius Minisart, Goettingen, Germany ) under low pressure, high-445 purity N2, and the filtered samples were stored in amber glass bottles at 4 °C in the dark until subsequent analysis. DOC measurements were carried out with a Shimadzu 5000A TOC Analyzer (Shimadzu, Kyoto, Japan) as described by [25], and concentrations were calculated according to [26].…”