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Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria

2015; Nature Portfolio; Volume: 526; Issue: 7574 Linguagem: Inglês

10.1038/nature15733

1476-4687

Gunter Wegener, Viola Krukenberg, Dietmar Riedel, Halina E. Tegetmeyer, Antje Boëtius,

Microbial metabolism and enzyme function

Marine anaerobic methanotrophic archaea and sulfate-reducing bacteria connect by pili-like nanowires, suggesting that direct interspecies exchange of electrons could be a fundamental mechanism in the anaerobic oxidation of methane. Anaerobic oxidation of methane in marine sediments, of central importance for the global methane cycle, is a collaborative process performed by consortia of methane-oxidizing archaea and sulfate-reducing bacteria. The biochemical basis of this syntrophic relationship is not fully understood. It has been suggested that exchange of a diffusible metabolite between the cooperating microbes is essential, but two groups reporting in this issue of Nature challenge this idea. Victoria Orphan and colleagues examined the biosynthetic activity at the single-cell level in microbial consortia prepared from sediment sampled from an active methane seep at Hydrate Ridge North in the Northwest Pacific. They find that cell activities are independent of the distance between syntrophic partners, which is inconsistent with a model involving the diffusion of intermediates over short distances. Instead, direct electron transfer between archaea and bacteria, mediated by large multi-haem cytochromes produced by ANME-2 archaea, is a central mechanism of their interaction. Gunter Wegener et al. show that interspecies exchange of electrons in microbial samples derived from hydrothermal vent sediments from Guaymas Basin in the Gulf of California is most probably through direct transfer of electrons by means of 'nanowires' connecting the two partners. These authors propose that electron transfer is mediated by pili-like structures and outer-membrane multi-haem cytochromes. The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor1,2. 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 zone3,4,5. 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 electrons7,8. 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 Geobacter9,10. 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.