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Worm tubes as conduits for the electrogenic microbial grid in marine sediments.

ABSTRACT: Electrogenic cable bacteria can couple spatially separated redox reaction zones in marine sediments using multicellular filaments as electron conductors. Reported as generally absent from disturbed sediments, we have found subsurface cable aggregations associated with tubes of the parchment worm Chaetopterus variopedatus in otherwise intensely bioturbated deposits. Cable bacteria tap into tubes, which act as oxygenated conduits, creating a three-dimensional conducting network extending decimeters into sulfidic deposits. By elevating pH, promoting Mn, Fe-oxide precipitation in tube linings, and depleting S around tubes, they enhance tube preservation and favorable biogeochemical conditions within the tube. The presence of disseminated filaments a few cells in length away from oxygenated interfaces and the reported ability of cable bacteria to use a range of redox reaction couples suggest that these microbes are ubiquitous facultative opportunists and that long filaments are an end-member morphological adaptation to relatively stable redox domains.

SUBMITTER: Aller RC

PROVIDER: S-EPMC6636988 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Worm tubes as conduits for the electrogenic microbial grid in marine sediments.

Aller Robert C RC Aller Josephine Y JY Zhu Qingzhi Q Heilbrun Christina C Klingensmith Isaac I Kaushik Aleya A

Science advances 20190717 7

Electrogenic cable bacteria can couple spatially separated redox reaction zones in marine sediments using multicellular filaments as electron conductors. Reported as generally absent from disturbed sediments, we have found subsurface cable aggregations associated with tubes of the parchment worm <i>Chaetopterus variopedatus</i> in otherwise intensely bioturbated deposits. Cable bacteria tap into tubes, which act as oxygenated conduits, creating a three-dimensional conducting network extending de ...[more]

PMID: 31328163

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Project description:Recently, a novel electrogenic type of sulphur oxidation was documented in marine sediments, whereby filamentous cable bacteria (Desulfobulbaceae) are mediating electron transport over cm-scale distances. These cable bacteria are capable of developing an extensive network within days, implying a highly efficient carbon acquisition strategy. Presently, the carbon metabolism of cable bacteria is unknown, and hence we adopted a multidisciplinary approach to study the carbon substrate utilization of both cable bacteria and associated microbial community in sediment incubations. Fluorescence in situ hybridization showed rapid downward growth of cable bacteria, concomitant with high rates of electrogenic sulphur oxidation, as quantified by microelectrode profiling. We studied heterotrophy and autotrophy by following (13)C-propionate and -bicarbonate incorporation into bacterial fatty acids. This biomarker analysis showed that propionate uptake was limited to fatty acid signatures typical for the genus Desulfobulbus. The nanoscale secondary ion mass spectrometry analysis confirmed heterotrophic rather than autotrophic growth of cable bacteria. Still, high bicarbonate uptake was observed in concert with the development of cable bacteria. Clone libraries of 16S complementary DNA showed numerous sequences associated to chemoautotrophic sulphur-oxidizing Epsilon- and Gammaproteobacteria, whereas (13)C-bicarbonate biomarker labelling suggested that these sulphur-oxidizing bacteria were active far below the oxygen penetration. A targeted manipulation experiment demonstrated that chemoautotrophic carbon fixation was tightly linked to the heterotrophic activity of the cable bacteria down to cm depth. Overall, the results suggest that electrogenic sulphur oxidation is performed by a microbial consortium, consisting of chemoorganotrophic cable bacteria and chemolithoautotrophic Epsilon- and Gammaproteobacteria. The metabolic linkage between these two groups is presently unknown and needs further study.

Project description:BackgroundMany animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species.ResultsIn this study on the obligate symbiosis between the gutless marine annelid Olavius algarvensis and its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80 O. algarvensis individuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of all O. algarvensis individuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted.ConclusionsWe hypothesize that variable degrees of fidelity are advantageous for O. algarvensis by allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources. Video Abstract.

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Worm tubes as conduits for the electrogenic microbial grid in marine sediments.

Publications

Worm tubes as conduits for the electrogenic microbial grid in marine sediments.

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