High pCO2-induced exopolysaccharide-rich ballasted aggregates of planktonic cyanobacteria could explain Paleoproterozoic carbon burial

Abstract

The contribution of planktonic cyanobacteria to burial of organic carbon in deep-sea sediments before the emergence of eukaryotic predators ~1.5 Ga has been considered negligible owing to the slow sinking speed of their small cells. However, global, highly positive excursion in carbon isotope values of inorganic carbonates ~2.22–2.06 Ga implies massive organic matter burial that had to be linked to oceanic cyanobacteria. Here to elucidate that link, we experiment with unicellular planktonic cyanobacteria acclimated to high partial CO2 pressure (pCO2) representative of the early Paleoproterozoic. We find that high pCO2 boosts generation of acidic extracellular polysaccharides (EPS) that adsorb Ca and Mg cations, support mineralization, and aggregate cells to form ballasted particles. The down flux of such self-assembled cyanobacterial aggregates would decouple the oxygenic photosynthesis from oxidative respiration at the ocean scale, drive export of organic matter from surface to deep ocean and sustain oxygenation of the planetary surface.

Sedimentation of ballasted cells‐free EPS in meromictic Fayetteville Green Lake

“…Similar, highly positive, excursion in carbon isotope values of inorganic carbonates (the ~2.22–2.06 Ga Lomagundi‐Jatuli carbon isotope anomaly) is recorded for sediments of the Paleoproterozoic ocean (Karhu & Holland, ; Planavsky, Bekker, Hofmann, Owens, & Lyons, ). Sedimentation of ballasted cyanobacterial EPS in FGL resembles the mechanism of biomass export, proposed for Paleoproterozoic (Kamennaya et al, ), though under high Paleoproterozoic‐like p CO 2 EPS‐bound cells aggregates rather than released EPS were proposed to drive the burial of cyanobacterial biomass. The two model studies—the earlier isolate study and the presented FGL‐enrichment study—independently indicate the key role of cyanobacterial EPS in biomass sedimentation in marine as well as in freshwater environments and imply that cyanobacterial EPS ballasting can be a universal trait of both modern and ancient aquatic systems.…”

“…In aquatic systems with low availability of organic carbon, EPS are products mainly of photosynthetic fixation of inorganic carbon (C i ) and their synthesis can be affected by the substrate concentration (DIC) and availability relative to the availability of other essential nutrients (Crosbie, Tuebner, and Weisse, (); Gordillo, Jiménez, Figueroa, & Niell, ; Otero & Vincenzini, ; De Philippis, Sili, & Vincenzini, ; Kamennaya et al, ; Kamennaya et al, ). The ambient DIC concentrations in FGL are relatively high (Table ) owing to an input of DIC‐rich groundwater (Havig et al, ; Takahashi et al, ).…”

“…When compared, a unit of Synechococci biomass can adsorb approximately 1.7 times more cations from FGL water than the equivalent biomass unit of a calcifying marine Synechococcus sp. strain PCC8806 from seawater (Kamennaya et al, ; Lee et al, ), suggesting that EPS of FGL Synechococci have high capacity for ballasting. Sorption of Ca and Mg cations alone increases the biomass density by ~0.23%.…”

“…In some case, EPS was associated with non-conductive presumably mineral material (h). Scale bar = 2 μm (a-c); 25 μm (c); 1 μm (d-f); 0.5 μm (g, h) nutrients (Crosbie, Tuebner, and Weisse, (2003); Gordillo, Jiménez, Figueroa, & Niell, 1998;Otero & Vincenzini, 2004;De Philippis, Sili, & Vincenzini, 1996;Kamennaya et al, 2015;Kamennaya et al, 2018). The ambient DIC concentrations in FGL are relatively high (Table 1) owing to an input of DIC-rich groundwater (Havig et al, 2018;Takahashi et al, 1968).…”

“…Second, we enriched FGL Synechococci and used this enrichment as a simplified model to study FGL epilimnion sedimentation. Third, using the microscopy-enhanced physiological analyses (Kamennaya et al, 2018) of the enrichment, we demonstrated Synechococci capacity to release EPS, EPS capacity to bind cations and to form ballasted aggregates under ambient as well as elevated pCO 2 conditions. Based on the above findings, we propose a model of cells-free cyanobacterial biomass sedimentation that explains the composition of FGL sediment.…”