Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria

Abstract

The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. In marine sediments, AOM is performed by dual-species consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) inhabiting the methane-sulfate transition zone. The biochemical pathways and biological adaptations enabling this globally relevant process are not fully understood. Here we study the syntrophic interaction in thermophilic AOM (TAOM) between ANME-1 archaea and their consortium partner SRB HotSeep-1 (ref. 6) at 60 °C to test the hypothesis of a direct interspecies exchange of electrons. The activity of TAOM consortia was compared to the first ANME-free culture of an AOM partner bacterium that grows using hydrogen as the sole electron donor. The thermophilic ANME-1 do not produce sufficient hydrogen to sustain the observed growth of the HotSeep-1 partner. Enhancing the growth of the HotSeep-1 partner by hydrogen addition represses methane oxidation and the metabolic activity of ANME-1. Further supporting the hypothesis of direct electron transfer between the partners, we observe that under TAOM conditions, both ANME and the HotSeep-1 bacteria overexpress genes for extracellular cytochrome production and form cell-to-cell connections that resemble the nanowire structures responsible for interspecies electron transfer between syntrophic consortia of Geobacter. HotSeep-1 highly expresses genes for pili production only during consortial growth using methane, and the nanowire-like structures are absent in HotSeep-1 cells isolated with hydrogen. These observations suggest that direct electron transfer is a principal mechanism in TAOM, which may also explain the enigmatic functioning and specificity of other methanotrophic ANME-SRB consortia.

Electrically Conductive Pili from Pilin Genes of Phylogenetically Diverse Microorganisms

“…e-Pili have been proposed to wire an anaerobic methane oxidizer of the ANME-1 phylogenetic group to the sulfate-reducer Desulfofervidus auxilii for DIET (Krukenberg et al 2016, Wegener et al 2015. It was not possible for us to obtain a sample of the consortium to directly evaluate the conductivity of the pili, but G. sulfurreducens readily expressed pili ( Figure 4D) from the Do.…”

“…For example, it was suggested that e-pili were involved in DIET in a consortium of an ANME-1 microbe and its sulfate-reducing partner (Wegener et al 2015). The sulfate-reducing partner highly expressed a pilin gene when the two microorganisms were growing syntrophically and pili-like filaments were abundant in the co-culture (Wegener et al 2015).…”

“…For example, it was suggested that e-pili were involved in DIET in a consortium of an ANME-1 microbe and its sulfate-reducing partner (Wegener et al 2015). The sulfate-reducing partner highly expressed a pilin gene when the two microorganisms were growing syntrophically and pili-like filaments were abundant in the co-culture (Wegener et al 2015). It was proposed that the pili of the sulfate reducer were conductive (Wegener et al 2015), but this was not verified, possibly due to difficulties in obtaining sufficient biomass.…”

Microbial nanowires: an electrifying tale

“…Apart from interspecies electron transfer, MNWs have also been implicated in electron transfer between bacteria and archaea (Wegener et al, 2015). Further, cyanobacteria are an important constituent of the microbial mat and it is hypothesized that cyanobacterial MNWs can transfer electrons to other micro-organisms present in the microbial mat (Gorby et al, 2006;Lea-Smith et al, 2015).…”

“…MNWs have been believed to play a role in methane production in syntrophic microbial communities (Morita et al, 2011;Rotaru et al, 2014;Summers et al, 2010;Wegener et al, 2015), which can be exploited further for improved methane production in anaerobic digesters. Interested readers are referred to specific reviews on this topic (Lovley, 2011;.…”