Efficient recycling of nutrients in modern and past hypersaline environments

Abstract

The biogeochemistry of hypersaline environments is strongly influenced by changes in biological processes and physicochemical parameters. Although massive evaporation events have occurred repeatedly throughout Earth history, their biogeochemical cycles and global impact remain poorly understood. Here, we provide the first nitrogen isotopic data for nutrients and chloropigments from modern shallow hypersaline environments (solar salterns, Trapani, Italy) and apply the obtained insights to δ 15 N signatures of the Messinian salinity crisis (MSC) in the late Miocene. Concentrations and δ 15 N of chlorophyll a , bacteriochlorophyll a , nitrate, and ammonium in benthic microbial mats indicate that inhibition of nitrification suppresses denitrification and anammox, resulting in efficient ammonium recycling within the mats and high primary productivity. We also suggest that the release of 15 N-depleted NH 3(gas) with increasing salinity enriches ammonium 15 N in surface brine (≈34.0‰). Such elevated δ 15 N is also recorded in geoporphyrins isolated from sediments of the MSC peak (≈20‰), reflecting ammonium supply sufficient for sustaining phototrophic primary production. We propose that efficient nutrient supply combined with frequent bottom-water anoxia and capping of organic-rich sediments by evaporites of the Mediterranean MSC could have contributed to atmospheric CO 2 reduction during the late Miocene.

Diazotrophy Drives Primary Production in the Organic-Rich Shales Deposited Under a Stratified Environment During the Messinian Salinity Crisis (Vena del Gesso, Italy)

“…Although much stronger density stratification formed in the Vena del Gesso basin should have resulted in slower ammonium supply rate compared to these modern analogs, the possibility of ammonium assimilation cannot be eliminated as we have no constraints on the depth of chemocline during the deposition of the PLG shales. It is noteworthy, however, that assimilation of subsurface ammonium by phototrophs during the MSC peak resulted in extremely elevated δ 15 N of geoporphyrins (Isaji et al, 2019), which highly contrasts with the results in this study (discussed in Section "Fluctuations in the Chemocline Depth Associating Shifts in the Nitrogen Cycle").…”

“…The substantial 13 C-depletion may be related with difference in carbon assimilation pathway of phototrophs, and/or difference in δ 13 C of source DIC which has depth and seasonal variabilities. Although specific source cannot be identified, brown-colored green sulfur bacteria can at least be excluded as the possible source of BiCAP-type porphyrins, because the δ 13 C values of isorenieratane, which has similar δ 13 C values to that of bacteriochlorophyll e (Ohkouchi et al, FIGURE 4 | The δ 15 N values of geoporphyrins compiled from previous studies (gray circles: Chicarelli et al, 1993;Ohkouchi et al, 2006;Kashiyama et al, 2008aKashiyama et al, ,b, 2010Higgins et al, 2012;Junium et al, 2015;Gueneli et al, 2018), those determined for the PLG shales in this study (pink circles), and those of the shale layers in the Realmonte salt mine in Sicily deposited during the MSC peak (blue circles: Isaji et al, 2019).…”

“…The PLG shales analyzed in this study were deposited when the chemocline was deep enough to induce nitrificationdenitrification (and/or anammox) coupling and a predominance of diazotrophic cyanobacteria, which is recorded as a specific δ 15 N range between −7 and −5 . Significantly, substantial elevation in δ 15 N values (≈20 ) are recorded in the geoporphyrins isolated from the mud-anhydrite layers deposited under density-stratified condition during the MSC peak (Figure 4; Isaji et al, 2019). This contrasting signal is interpreted to reflect the assimilation of 15 N-enriched ammonium pools from the subsurface and the recycling of bioavailable nitrogen within the water column with shallow chemocline (Figure 5B).…”

“…Important processes are indicated by red arrows. (B) Proposed nitrogen cycle under reduced freshwater input during the MSC peak (Isaji et al, 2019). The shallow chemocline results in phototrophic assimilation of the subsurface ammonium rather than nitrification followed by denitrification (and/or anammox).…”

“…Moreover, the carbon and nitrogen isotopic compositions of geoporphyrins retain the original signals of the chloropigments, which strongly reflect those of the source phototrophs Ohkouchi et al, 2006Ohkouchi et al, , 2008Higgins et al, 2011). Therefore, structural and isotopic information of geoporphyrins in the geological samples provide us insights into phototrophic community as well as carbon and nitrogen cycles of past environments (Hayes et al, 1987;Boreham et al, 1989Boreham et al, , 1990Ocampo et al, 1989;Popp et al, 1989;Chicarelli et al, 1993;Keely et al, 1994;Ohkouchi et al, 2006Ohkouchi et al, , 2015Kashiyama et al, 2008aKashiyama et al, ,b, 2010Higgins et al, 2012;Junium et al, 2015;Gueneli et al, 2018;Isaji et al, 2019). Importantly, geoporphyrins in marine sediments are mostly derived from marine phototrophs, because the turnover rate of aquatic chlorophylls are substantially faster than that of terrestrial chlorophylls (Hendry et al, 1987), and most chlorophylls produced by the terrestrial plants are enzymatically decomposed during senescence of the leaf (e.g., Matile et al, 1996), degraded by bacteria in soils (Hoyt, 1966), and readily oxidized during transport (Sanger, 1988).…”