Conductive Particles Enable Syntrophic Acetate Oxidation between Geobacter and Methanosarcina from Coastal Sediments

Abstract

Coastal sediments are rich in conductive particles, possibly affecting microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure, and their survival depends on successful partnership. Here, we demonstrate that conductive particles enable the partnership between SAO bacteria (i.e., Geobacter spp.) and methanogens (Methanosarcina spp.) from the coastal sediments of the Bothnian Bay of the Baltic Sea. Baltic methanogenic sediments were rich in conductive minerals, had an apparent isotopic fractionation characteristic of CO2-reductive methanogenesis, and were inhabited by Geobacter and Methanosarcina. As long as conductive particles were delivered, Geobacter and Methanosarcina persisted, whereas exclusion of conductive particles led to the extinction of Geobacter. Baltic Geobacter did not establish a direct electric contact with Methanosarcina, necessitating conductive particles as electrical conduits. Within SAO consortia, Geobacter was an efficient [13C]acetate utilizer, accounting for 82% of the assimilation and 27% of the breakdown of acetate. Geobacter benefits from the association with the methanogen, because in the absence of an electron acceptor it can use Methanosarcina as a terminal electron sink. Consequently, inhibition of methanogenesis constrained the SAO activity of Geobacter as well. A potential benefit for Methanosarcina partnering with Geobacter is that together they competitively exclude acetoclastic methanogens like Methanothrix from an environment rich in conductive particles. Conductive particle-mediated SAO could explain the abundance of acetate oxidizers like Geobacter in the methanogenic zone of sediments where no electron acceptors other than CO2 are available.

Influence of electron acceptor availability and microbial community structure on sedimentary methane oxidation in a boreal estuary

“…However, in environments with Fe 3? reducing bacteria and conductive minerals such as in iron-rich sediments of our study sites, Methanosaetaceae and Methanosarcinaceae could also drive CO 2 -reduction (to CH 4 ) coupled with either direct or indirect (via conductive materials) electron transfer from iron-reducing bacteria, such as Geobacter (Rotaru et al 2014(Rotaru et al , 2018. Some metagenomic datasets also indicate Bathyarchaeota, which were dominant archaea both at our study sites and Bothnian Sea sediments (Rasigraf et al 2019) ( Supplementary Fig.…”

Extracellular Electron Uptake by TwoMethanosarcinaSpecies

“…For instance, co-cultures of G. metallireducens and M. barkeri were stimulated at the addition of conductive particles, such as GAC (Liu et al, 2012), carbon cloth (Chen et al, 2014a), biochar (Chen et al, 2014b), or magnetite (Wang et al, 2018). On the other hand, the addition of non-conductive materials did not stimulate DIET (Chen et al, 2014a; Rotaru et al, 2018a). In addition, conductive particles appear to play a significant role in interspecies interactions from natural and artificial ecosystems such as sediments, soils, rice paddies or anaerobic digesters (Holmes et al, 2017a; Rotaru et al, 2018b; Ye et al, 2018; Zhang et al, 2018).…”

“…In addition, conductive particles appear to play a significant role in interspecies interactions from natural and artificial ecosystems such as sediments, soils, rice paddies or anaerobic digesters (Holmes et al, 2017a; Rotaru et al, 2018b; Ye et al, 2018; Zhang et al, 2018). In these cases, the addition of conductive particles enriched for DIET-related Methanosarcinales (Dang et al, 2016; Holmes et al, 2017b; Rotaru et al, 2018a; Zheng et al, 2015). However, exceptions were observed since occasionally conductive particles enriched for H2-utilizing methanogens of the genus Methanospirillum (Lee et al, 2016) or Methanobacterium (Lin et al, 2017; Zhuang et al, 2015).…”

Extracellular Electron Uptake by Two Methanosarcina Species

“…For instance, cocultures of G. metallireducens and M. barkeri were stimulated at the addition of conductive particles, such as GAC (Liu et al, 2012), carbon cloth (Chen et al, 2014a), biochar (Chen et al, 2014b), or magnetite (Wang et al, 2018). On the other hand, the addition of non-conductive materials did not stimulate DIET (Chen et al, 2014a;Rotaru et al, 2018a). In addition, conductive particles appear to play a significant role in interspecies interactions from natural and artificial ecosystems such as sediments, soils, rice paddies or anaerobic digesters (Holmes et al, 2017a;Rotaru et al, 2018b;Ye et al, 2018;Zhang L. et al, 2018a).…”

“…In addition, conductive particles appear to play a significant role in interspecies interactions from natural and artificial ecosystems such as sediments, soils, rice paddies or anaerobic digesters (Holmes et al, 2017a;Rotaru et al, 2018b;Ye et al, 2018;Zhang L. et al, 2018a). In these cases, the addition of conductive particles enriched for DIET-related Methanosarcinales (Zheng et al, 2015;Dang et al, 2016;Holmes et al, 2018b;Rotaru et al, 2018a). However, exceptions were observed since occasionally conductive particles enriched for H 2 -utilizing methanogens of the genus Methanospirillum (Lee et al, 2016) or Methanobacterium (Zhuang et al, 2015;Lin et al, 2017).…”