Fermentation and Anaerobic Oxidation of Organic Carbon in the Oxygen Minimum Zone of the Upwelling Ecosystem Off Concepción, in Central Chile

Benjamín M Srain,Laura Farías,Alex Schwarz,Silvio Pantoja-Gutiérrez,Marcus Sobarzo,Humberto E González,Giovanni Testa,Norma Pérez,Giovanni Daneri

doi:10.3389/fmars.2020.00533

Abstract

We studied dynamic of fermentation and anaerobic degradation of organic matter in the Oxygen Minimum Zone (OMZ) of the Humboldt Current System by analyzing products of main anaerobic microbial reactions (fermentation, denitrification, and reduction of Fe(III)s and SO42-) during laboratory incubations of OMZ waters and in the water column during a year cycle. Fermentation of glucose and amino acids resulted in production of volatile fatty acids, mainly acetate, that were detected year-round and associated to high primary production rates, dissolved organic carbon (DOC) increase, and presence of Equatorial Sub Surface anoxic waters at the sampling site off Concepción in central Chile. While ethanol was produced from glucose fermentation by OMZ water microbes, it was not detected in the water column. Ammonium produced by fermentation of amino acids during anoxic represents a source of NH4+ that could explain previously unaccounted for NH4+ requirements for anammox bacteria and microaerophilic NH4+ oxidizer Thaumarchaeota in anoxic marine ecosystems. Evidence of thermodynamically feasible acetate oxidation with Fe(III)s as electron acceptor unveils microbial ability to reduce solid-phase iron carried by rivers using fermented metabolites in oxygen-depleted water, thus releasing dissolved bioavailable Fe. We evidenced that products of fermentation are advected to oxygenated waters of Sub Antarctic origin during austral winter intrusion and potentially supplying C, N and electron sources, a process likely to be enhanced due to both thermodynamically (temperature) and kinetic (organic load) decrease in O2 during the XXI century.

Highlights

Hypoxic zones within the marine water column appear to be expanding due to warming and eutrophication (Diaz and Rosenberg, 2008; Rabalais et al, 2014; Schmidtko et al, 2017)
No decay of fermentation products was detected in 7 days of incubation likely due either to the absence of external electron acceptors for anaerobic oxidation in the culture media, the thermodynamically unfavorable conditions caused by buildup of fermentation products, or the slow growth rates of acetate consumers suggested by comparing decay of amino acids (90% in near 2 days, Figure 2B) with decay of acetate (90% in near 30 days, Figures 2C–E)
Microbial oxidation of acetate with excess NO3− (Figure 2C), Fe(OH)3 (Figure 2D), and SO42− as electron acceptors was detected in the inocula treatments of Oxygen Minimum Zone (OMZ) water incubated under anaerobic conditions (Figure 2E)

Summary

Introduction

Hypoxic zones within the marine water column appear to be expanding due to warming and eutrophication (Diaz and Rosenberg, 2008; Rabalais et al, 2014; Schmidtko et al, 2017) These processes will enhance fermentative production of semi-reduced metabolites that act as substrates for anaerobic microbial oxidation of organic matter (Oremland and Polcin, 1982; Megonigal et al, 2004) through, for example, NO3− (denitrification) and SO42− reduction, and methanogenesis (Sansone and Martens, 1981; Jørgensen, 1982). O2depleted marine environments are typically found in sediments, enclosed or semi-enclosed water bodies, coastal ocean dead zones, and areas referred to as Oxygen Minimum Zones or OMZs (Helly and Levin, 2004; Diaz and Rosenberg, 2008). Interest in fermentative reactions is becoming more relevant in light of expansion of OMZs (Breitburg et al, 2018), and the increasing concentrations of N (Howarth, 2008), P (Bennett et al, 2001), and organic carbon (Berner, 1982) associated with eutrophication and deoxygenation of the coastal ocean (Rabalais et al, 2014)

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Conclusion