The possible occurrence of iron-dependent anaerobic methane oxidation in an Archean Ocean analogue

Abstract

In the ferruginous and anoxic early Earth oceans, photoferrotrophy drove most of the biological production before the advent of oxygenic photosynthesis, but its association with ferric iron (Fe³⁺) dependent anaerobic methane (CH₄) oxidation (AOM) has been poorly investigated. We studied AOM in Kabuno Bay, a modern analogue to the Archean Ocean (anoxic bottom waters and dissolved Fe concentrations > 600 µmol L^-1). Aerobic and anaerobic CH₄ oxidation rates up to 0.12 ± 0.03 and 51 ± 1 µmol L^-1 d^-1, respectively, were put in evidence. In the Fe oxidation-reduction zone, we observed high concentration of Bacteriochlorophyll e (biomarker of the anoxygenic photoautotrophs), which co-occurred with the maximum CH₄ oxidation peaks, and a high abundance of Candidatus Methanoperedens, which can couple AOM to Fe³⁺ reduction. In addition, comparison of measured CH₄ oxidation rates with electron acceptor fluxes suggest that AOM could mainly rely on Fe³⁺ produced by photoferrotrophs. Further experiments specifically targeted to investigate the interactions between photoferrotrophs and AOM would be of considerable interest. Indeed, ferric Fe³⁺-driven AOM has been poorly envisaged as a possible metabolic process in the Archean ocean, but this can potentially change the conceptualization and modelling of metabolic and geochemical processes controlling climate conditions in the Early Earth.

Figure 1

Physico-chemical conditions in Kabuno Bay are analogous to the Archean Ocean (a,b: May 2013; c,d: September 2013; e,f: August 2014). (a,c,e): bacteriochlorophyll contents (Bchle, µg L⁻¹), dissolved oxygen (DO, µmol L⁻¹) and CH₄ concentrations (µmol L⁻¹), specific conductivity (SPC, µS cm⁻¹). (b,d,f): methane oxidation rates (µmol L⁻¹ d⁻¹) without molybdate added (− Mo) and with molybdate added (+ Mo).

Figure 2

Vertical profiles of electron acceptors potentially involved in AOM (a–c: May 2013; d–g: September 2013; h–k: August 2014). (d,h): NOx and NH₄⁺ concentrations (µmol L⁻¹). (a,e,i): SO₄²⁻ and HS⁻ concentrations (µmol L⁻¹). (b,f,j(: particulate (MnO₂) and dissolved (Mn²⁺) Mn concentrations (µmol L⁻¹). (c,g,k(: particulate (Fe³⁺) and dissolved (Fe²⁺) Fe concentrations (µmol L⁻¹).

Figure 3

Presence of Candidatus Methanoperedens, capable of Fe-related AOM. 16S rRNA gene phylogenetic tree of the Candidatus Methanoperedens representative related OTUs (0.03 cut-off; only those OTUs containing more than 10 reads are shown) retrieved by pyrosequencing from Kabuno Bay water samples, the scale bar indicates 0.10 fixed point mutation per nucleotide position.

Figure 4

Co-occurence of Candidatus methanoperedens and ferrophototrophs in the chemocline of Kabuno Bay. (a) Vertical distribution of Candidatus methanoperedens and (b), Vertical profiles of particulate Fe concentrations (µmol L⁻¹) and Bacteriochlorophyll e (Bchle) content (µg L⁻¹) in February 2012. While this profile was not contemporary to the measurements of AOM (Fig. 1) the particulate Fe and Bacteriochlorophyll e peaks show that AOM and Archaea abundance coincided.

Figure 5

Chemical evidence of Fe³⁺ as an important electron acceptor of AOM. Fraction (%) of the integrated AOM rates potentially sustained by Fe reduction, NO₃⁻ reduction and SO₄²⁻ reduction rates measured by Llirós et al. and Michiels et al.. Error bars are calculated as the standard deviation of the mean of the three sampling campaigns.

Figure 6

Potential role of iron-oxide AOM in Archean Ocean metabolism. In the Archean Ocean, anaerobic metabolism (photoferrotrophy, methanogenesis and CO-acetogenesis in dark blue) dominated before the advent of oxygenic photosynthesis (in light blue). In red, we propose anaerobic methane oxidation (AOM) using Fe oxides as electron acceptor as additional metabolic process. Before the advent of oxygenic photosynthesis, Fe³⁺ dependent AOM linked photoferrotrophy and H₂-methanogenesis that so far have been seen as two parallel and unconnected processes. After the advent of oxygenic photosynthesis, Fe oxides-dependent AOM might have used the abundantly produced Fe(OH)₃ from the oxidation of Fe²⁺ by O₂ to further remove CH₄ from the water column, facilitating the increase of O₂ in the atmosphere and the great oxidation event.