High dark inorganic carbon fixation rates by specific microbial groups in the Atlantic off the Galician coast (NW Iberian margin)

Abstract

Bulk dark dissolved inorganic carbon (DIC) fixation rates were determined and compared to microbial heterotrophic production in subsurface, meso- and bathypelagic Atlantic waters off the Galician coast (NW Iberian margin). DIC fixation rates were slightly higher than heterotrophic production throughout the water column, however, more prominently in the bathypelagic waters. Microautoradiography combined with catalyzed reporter deposition fluorescence in situ hybridization (MICRO-CARD-FISH) allowed us to identify several microbial groups involved in dark DIC uptake. The contribution of SAR406 (Marinimicrobia), SAR324 (Deltaproteobacteria) and Alteromonas (Gammaproteobacteria) to the dark DIC fixation was significantly higher than that of SAR202 (Chloroflexi) and Thaumarchaeota, in agreement with their contribution to microbial abundance. Q-PCR on the gene encoding for the ammonia monooxygenase subunit A (amoA) from the putatively high versus low ammonia concentration ecotypes revealed their depth-stratified distribution pattern. Taken together, our results indicate that chemoautotrophy is widespread among microbes in the dark ocean, particularly in bathypelagic waters. This chemolithoautotrophic biomass production in the dark ocean, depleted in bio-available organic matter, might play a substantial role in sustaining the dark ocean's food web.

Linking Uncultivated Microbial Populations and Benthic Carbon Turnover by Using Quantitative Stable Isotope Probing

“…However, metagenomic data have shown that the RBG-2 and RBG-1351 groups, belonging to the GIF9 and GIF3 orders (formerly classes) of Chloroflexi, respectively, may be capable of chemoautotrophic growth via the Wood-Ljungdahl pathway (35). In addition, some members of the SAR202 clade in the dark ocean had low levels of DIC uptake, as determined by catalyzed reporter deposition–fluorescence in situ hybridization combined with microautoradiography (MICRO-CARD-FISH) (38). There are also studies reporting their utilization of labile and recalcitrant organic compounds (39).…”

Carbon recycling efficiency and phosphate turnover by marine nitrifying archaea

“…450 days; Table 3). The rates and yields reported for N. maritimus cultures in the current study represent an incremental step toward modeling bathypelagic chemoautotrophs, who operate at lower temperature, higher pressure, and may use other reduced substrates [e.g., (10,33)]. At present, our empirical evidence recommends that biogeochemical budgets include chemoautotrophic recycling fluxes driven by reduced N that mitigate at least 4.5% of detrital organic C respiration and transform 4.3% of detrital P into new P substrates.…”

“…Ship-board radiotracer incubations of bathypelagic microbes suggest that dark ocean chemoautotrophy ranges from 0.8 to 1.2 Pg C year −1 (2,5,6), but these estimates are >100% higher than geochemical mass balance estimates, which range up to 0.4 Pg C year −1 (7) and have assumed (i) complete oxidation of organic nitrogen (N) sinking below the euphotic zone and (ii) a C yield from nitrification of 10% [C 0 /N n = 0.1; Nitrosomonas marina; (8,9)]. This discrepancy has been explained by missing transport of reduced N into the bathypelagic or alternative energy sources to support dark ocean chemoautotrophy (2,6,7,10). However, in theory, C fixation by the 3-hydroxypropionate/4-hydroxybutyrate (HP/HB) pathway should lower the adenonine 5′-triphosphate (ATP) demand of thaumarchaea (4) and thus translate to a higher C yield for archaeal nitrification.…”

Grand Challenges in Microbe-Driven Marine Carbon Cycling Research

“…They not only play a key role in sustaining the chemosynthetic ecosystems related to deep-sea hydrothermal vents and cold seeps (McNichol et al, 2018;Dick, 2019) but also may contribute significantly to food web and energy transfer in non-extreme environments (Herndl and Reinthaler, 2013). Dark carbon fixation may provide substantial primary production in certain marine waters (Taylor et al, 2001;Yakimov et al, 2011;Celussi et al, 2017;Guerrero-Feijóo et al, 2018;La Cono et al, 2018). Microbial degradation and remineralization of marine particulate organic matter (POM) significantly lower the BCP efficiency (Turner, 2015;Dang and Lovell, 2016).…”