Cable bacteria reduce methane emissions from rice-vegetated soils

Scholz, Vincent V.; Nielsen, Lars Peter; Risgaard-Petersen, Nils

doi:10.1038/s41467-020-15812-w

Cited by 76 publications

(28 citation statements)

References 29 publications

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“…Furthermore, inoculation of cable bacteria in rice pots has been found to reduce methane emissions (Scholz et al ., 2020 ). We show that cable bacteria grow in rice fields in Asia and the USA, which expands the known habitats of cable bacteria.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, cable bacteria have been found in mangrove sediments (Burdorf et al ., 2016 ) and around oxygen‐releasing roots of seagrass (Martin et al ., 2019 , 2018a ), saltmarsh Salicornia europaea , freshwater plants (including Littorella uniflora and Lobelia cardinalis ) and rice (Scholz et al ., 2019 ). It has been proposed that this may protect the roots against sulfide intrusion (Martin et al ., 2018a ) and indirectly suppress methane emissions (Scholz et al ., 2020 ). The studies that investigate cable bacteria around roots of aquatic plants have so far been predominantly based on laboratory grown plants (Martin et al ., 2018a ; Scholz et al ., 2020 , 2019 ) and the natural occurrence of plant‐associated cable bacteria is unknown.…”

Section: Introductionmentioning

confidence: 99%

“…It has been proposed that this may protect the roots against sulfide intrusion (Martin et al ., 2018a ) and indirectly suppress methane emissions (Scholz et al ., 2020 ). The studies that investigate cable bacteria around roots of aquatic plants have so far been predominantly based on laboratory grown plants (Martin et al ., 2018a ; Scholz et al ., 2020 , 2019 ) and the natural occurrence of plant‐associated cable bacteria is unknown.…”

Section: Introductionmentioning

confidence: 99%

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Cable bacteria at oxygen‐releasing roots of aquatic plants: a widespread and diverse plant–microbe association

et al. 2021

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Cable bacteria are sulfide-oxidising, filamentous bacteria that reduce toxic sulfide levels, suppress methane emissions and drive nutrient and carbon cycling in sediments. Recently, cable bacteria have been found associated with roots of aquatic plants and rice (Oryza sativa). However, the extent to which cable bacteria are associated with aquatic plants in nature remains unexplored.Using newly generated and public 16S rRNA gene sequence datasets combined with fluorescence in situ hybridisation, we investigated the distribution of cable bacteria around the roots of aquatic plants, encompassing seagrass (including seagrass seedlings), rice, freshwater and saltmarsh plants.Diverse cable bacteria were found associated with roots of 16 out of 28 plant species and at 36 out of 55 investigated sites, across four continents. Plant-associated cable bacteria were confirmed across a variety of ecosystems, including marine coastal environments, estuaries, freshwater streams, isolated pristine lakes and intensive agricultural systems. This pattern indicates that this plant-microbe relationship is globally widespread and neither obligate nor species specific.The occurrence of cable bacteria in plant rhizospheres may be of general importance to vegetation vitality, primary productivity, coastal restoration practices and greenhouse gas balance of rice fields and wetlands.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Cable bacteria at oxygen‐releasing roots of aquatic plants: a widespread and diverse plant–microbe association

et al. 2021

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“…Since their discovery, cable bacteria have been found at the oxic-anoxic interface in a wide range of aquatic sediment environments, including marine (e.g., Malkin et al, 2014 ; Burdorf et al, 2017 ), freshwater ( Risgaard-Petersen et al, 2015 ), and aquifer ( Müller et al, 2016 ) sediments. In these environments, cable bacteria strongly influence the elemental cycling of sulfur, iron, phosphorus, and methane ( Risgaard-Petersen et al, 2012 ; Seitaj et al, 2015 ; Sulu-Gambari et al, 2016 ; Scholz et al, 2020 ). Additionally, cable bacteria have been found attached to the anode of a benthic microbial fuel cell placed in anaerobic conditions ( Reimers et al, 2017 ) or in association with oxygenated zones around plant roots ( Scholz et al, 2019 ) and worm tubes in marine sediments ( Aller et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Cell Cycle, Filament Growth and Synchronized Cell Division in Multicellular Cable Bacteria

et al. 2021

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Cable bacteria are multicellular, Gram-negative filamentous bacteria that display a unique division of metabolic labor between cells. Cells in deeper sediment layers are oxidizing sulfide, while cells in the surface layers of the sediment are reducing oxygen. The electrical coupling of these two redox half reactions is ensured via long-distance electron transport through a network of conductive fibers that run in the shared cell envelope of the centimeter-long filament. Here we investigate how this unique electrogenic metabolism is linked to filament growth and cell division. Combining dual-label stable isotope probing (13C and 15N), nanoscale secondary ion mass spectrometry, fluorescence microscopy and genome analysis, we find that the cell cycle of cable bacteria cells is highly comparable to that of other, single-celled Gram-negative bacteria. However, the timing of cell growth and division appears to be tightly and uniquely controlled by long-distance electron transport, as cell division within an individual filament shows a remarkable synchronicity that extends over a millimeter length scale. To explain this, we propose the “oxygen pacemaker” model in which a filament only grows when performing long-distance transport, and the latter is only possible when a filament has access to oxygen so it can discharge electrons from its internal electrical network.

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“…Cable bacteria are found in such diverse environments because the spatial separation of redox half-reactions allows them to oxidize sulfide over a wide range of sediment depths (Meysman, 2018). This was recently illustrated when rice-vegetated soils were inoculated once with cable bacteria, which resulted in the successful establishment of a cable bacteria culture with a filament density that was comparable to those observed in marine or freshwater sediments (Scholz et al, 2020). Thus, cable bacteria can quickly colonize a habitat once conditions are favorable because of their capacity for LDET which gives them a competitive advantage over other, single-celled sulfide-oxidizing bacteria (Meysman, 2018).…”

Section: The Global Distribution Of Cable Bacteriamentioning

confidence: 99%

The ecophysiology of multicellular cable bacteria: insights from single cell imaging techniques

Geerlings¹

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Cable bacteria are multicellular, filamentous microorganisms that are capable of transporting electrons over centimeter-scale distances. Although recently discovered, these bacteria appear to be widely present in the seafloor, and when active, they exert a strong imprint on the local geochemistry. In particular, their electrogenic metabolism induces unusually strong pH excursions in aquatic sediments, which induces considerable mineral dissolution, and subsequent mineral re-precipitation. However at present, it is unknown whether and how cable bacteria play an active or direct role in the mineral re-precipitation process. To this end we present an explorative study of the formation of sedimentary minerals in and near filamentous cable bacteria using a combined approach of electron microscopy and spectroscopic techniques. Our observations reveal the formation of polyphosphate granules within the cells and two different types of biomineral formation directly associated with multicellular filaments of these cable bacteria: the attachment and incorporation of clay particles in a coating surrounding the bacteria, and encrustation of the cell envelope by iron minerals. These findings suggest a complex interaction between cable bacteria and the surrounding sediment matrix, and a substantial imprint of the electrogenic metabolism on mineral diagenesis and sedimentary biogeochemical cycling. Particularly the encrustation process leaves many open questions for further research. For example, we hypothesize that the complete encrustation of filaments might create a diffusion barrier and negatively impact the metabolism of the cable bacteria.

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Cable bacteria reduce methane emissions from rice-vegetated soils

Cited by 76 publications

References 29 publications

Cable bacteria at oxygen‐releasing roots of aquatic plants: a widespread and diverse plant–microbe association

Cable bacteria at oxygen‐releasing roots of aquatic plants: a widespread and diverse plant–microbe association

Cell Cycle, Filament Growth and Synchronized Cell Division in Multicellular Cable Bacteria

The ecophysiology of multicellular cable bacteria: insights from single cell imaging techniques

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