Worm tubes as conduits for the electrogenic microbial grid in marine sediments.
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ABSTRACT:
SUBMITTER: Aller RC
PROVIDER: S-EPMC6636988 | biostudies-literature |
REPOSITORIES: biostudies-literature
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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.
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Project description:The housing tube material of the marine worm Chaetopterus sp. exhibits thermal stability up to 250°C, similar to other biological materials such as mulberry silkworm cocoons. Interestingly, however, dynamic mechanical thermal analysis conducted in both air and water elucidated the lack of a glass transition in the organic tube wall material. In fact, the viscoelastic properties of the anhydrous and undried tube were remarkably stable (i.e. constant and reversible) between -75°C and 200°C in air, and 5°C and 75°C in water, respectively. Moreover, it was found that hydration and associated-water plasticization were key to the rubber-like flexible properties of the tube; dehydration transformed the material behaviour to glass-like. The tube is made of bionanocomposite fibrils in highly oriented arrangement, which we argue favours the biomaterial to be highly crystalline or cross-linked, with extensive hydrogen and/or covalent bonds. Mechanical property characterization in the longitudinal and transverse directions ascertained that the tubes were not quasi-isotropic structures. In general, the higher stiffness and strength in the transverse direction implied that there were more nanofibrils orientated at ± 45° and ± 65° than at 0° to the tube axis. The order of the mechanical properties of the soft-tough tubes was similar to synthetic rubber-like elastomers and even some viscid silks. The complex structure-property relations observed indicated that the worm has evolved to produce a tubular housing structure which can (i) function stably over a broad range of temperatures, (ii) endure mechanical stresses from specific planes/axes, and (iii) facilitate rapid growth or repair.
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Project description:Methanol is an ubiquitous compound that plays a role in microbial processes as a carbon and energy source, intermediate in metabolic processes or as end product in fermentation. In anoxic environments, methanol can act as the sole carbon and energy source for several guilds of microorganisms: sulfate-reducing microorganisms, nitrate-reducing microorganisms, acetogens and methanogens. In marine sediments, these guilds compete for methanol as their common substrate, employing different biochemical pathways. In this review, we will give an overview of current knowledge of the various ways in which methanol reaches marine sediments, the ecology of microorganisms capable of utilizing methanol and their metabolism. Furthermore, through a metagenomic analysis, we shed light on the unknown diversity of methanol utilizers in marine sediments which is yet to be explored.
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Project description:Disturbance strongly impacts patterns of community diversity, yet the shape of the diversity-disturbance relationship remains a matter of debate. The topic has been of interest in theoretical ecology for decades as it has practical implications for the understanding of ecosystem services in nature. One of these processes is the remineralization of organic matter by microorganisms in coastal marine sediments, which are periodically impacted by disturbances across the sediment-water interface. Here we set up an experiment to test the hypothesis that disturbance impacts microbial diversity and function during the anaerobic degradation of organic matter in coastal sediments. We show that during the first 3 weeks of the experiment, disturbance increased both microbial production, derived from the increase in microbial abundance, and diversity of the active fraction of the community. Both community diversity and phylogenetic diversity increased, which suggests that disturbance promoted the cohabitation of ecologically different microorganisms. Metagenome analysis also showed that disturbance increased the relative abundance of genes diagnostic of metabolism associated with the sequential anaerobic degradation of organic matter. However, community composition was not impacted in a systematic way and changed over time. In nature, we can hypothesize that moderate storm disturbances, which impact coastal sediments, promote diverse, and productive communities. These events, rather than altering the decomposition of organic matter, may increase the substrate turnover and, ultimately, remineralization rates.
| S-EPMC5133735 | biostudies-literature
Project description:PurposeThe aim of the present work was to assess the electrogenic activity of bacteria from hydrothermal vent sediments achieved under sulfate reducing (SR) conditions in a microbial fuel cell design with acetate, propionate and butyrate as electron donors.MethodsTwo different mixtures of volatile fatty acids (VFA) were evaluated as the carbon source at two chemical oxygen demand (COD) proportions. The mixtures of VFA used were: acetate, propionate and butyrate COD: 3:0.5:0.5 (stage 1) and acetate - butyrate COD: 3.5:0.5 (stage 2). Periodical analysis of sulfate (SO4 -2), sulfide (HS-) and COD were conducted to assess sulfate reduction (SR) and COD removal along with measurements of voltage and current to assess the global performance of the consortium in the system.ResultsPercentage of SR was of 97.5 ± 0.7 and 74.3 ± 1.5% for stage 1 and 2, respectively. The % COD removal was of 91 ± 2.1 and 75.3 ± 9.6 for stage 1 and 2, respectively. Although SR and COD removal were higher at stage 1, in regards of energy, stage 2 presented higher current and power densities and Coulombic efficiency as follows: 741.7 ± 30.5 μA/m2, 376 ± 34.4 μW/m2 and 5 ± 2.7%, whereas for stage 1 these values were: 419 ± 71 μA/m2, 52.7 ± 18 μW/m2 and 0.02%, respectively. A metagenomic analysis - stage 2 - in the anodic chamber, demonstrated that SR was due to Dethiosulfovibrionaceae (HA73), Desulfobacter and Desulfococcus and the electrogenic microorganisms were Planococcus, SHD-231, Proteiniclasticum, vadinCA02, and families Porphyromonadacea and Pseudomonadaceae.ConclusionsIt was demonstrated that microorganisms prevenient from hydrothermal vent sediments adapted to a microbial fuel cell system are able to generate electricity coupled to 74.3 ± 1.5 and 75.3 ± 9.6% of SR and COD removal respectively, with a mixture of acetate - butyrate.
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Project description:Invasive plants have extensive impacts on ecosystem function and biodiversity globally. Our inability to manage invasive species stems in part from a lack of understanding of the processes that control their successful establishment and spread. To date, studies have largely considered how above-ground processes control native/invasive plant interactions. Emerging research from terrestrial and wetland ecosystems demonstrates that below-ground processes under microbial control can determine the outcome of interactions between native and invasive plants. Whether sediment microbes modify the success of invasive macrophytes in marine ecosystems is untested, despite marine sediment microbes controlling many ecological processes (e.g. nutrient cycling) comparable to those in terrestrial ecosystems. We first show that sediment bacterial communities differ between the native seagrass Zostera capricorni and the invasive alga Caulerpa taxifolia and that those differences relate to functional changes in sulfur cycling between the macrophytes. Second, by experimentally manipulating the microbial communities we show that intact microbial communities in Z. capricorni sediments provide biotic resistance by reducing C. taxifolia fragment growth 119% compared to when they are inactive, and intact microbial communities in C. taxifolia sediments have positive feedbacks by increasing fragment growth 200%. Thus, similar to terrestrial ecosystems, microorganisms appear to indirectly control the success of invasive macrophytes in marine ecosystems.
| S-EPMC5575248 | biostudies-literature
Project description:Almost the entire seafloor is covered with sediments that can be more than 10 000 m thick and represent a vast microbial ecosystem that is a major component of Earth's element and energy cycles. Notably, a significant proportion of microbial life in marine sediments can exploit energy conserved during transformations of sulfur compounds among different redox states. Sulfur cycling, which is primarily driven by sulfate reduction, is tightly interwoven with other important element cycles (carbon, nitrogen, iron, manganese) and therefore has profound implications for both cellular- and ecosystem-level processes. Sulfur-transforming microorganisms have evolved diverse genetic, metabolic, and in some cases, peculiar phenotypic features to fill an array of ecological niches in marine sediments. Here, we review recent and selected findings on the microbial guilds that are involved in the transformation of different sulfur compounds in marine sediments and emphasise how these are interlinked and have a major influence on ecology and biogeochemistry in the seafloor. Extraordinary discoveries have increased our knowledge on microbial sulfur cycling, mainly in sulfate-rich surface sediments, yet many questions remain regarding how sulfur redox processes may sustain the deep-subsurface biosphere and the impact of organic sulfur compounds on the marine sulfur cycle.
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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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Project description:The ecology of aerobic microorganisms is never explored in marine oxygen minimum zone (OMZ) sediments. Here we reveal aerobic bacterial communities along ?3 m sediment-horizons of the eastern Arabian Sea OMZ. Sulfide-containing sediment-cores retrieved from 530 mbsl (meters beneath the sea-level) and 580 mbsl were explored at 15-30 cm intervals, using metagenomics, pure-culture-isolation, genomics and metatranscriptomics. Genes for aerobic respiration, and oxidation of methane/ammonia/alcohols/thiosulfate/sulfite/organosulfur-compounds, were detected in the metagenomes from all 25 sediment-samples explored. Most probable numbers for aerobic chemolithoautotrophs and chemoorganoheterotrophs at individual sample-sites were up to 1.1 × 107 (g sediment)-1. The sediment-sample collected from 275 cmbsf (centimeters beneath the seafloor) of the 530-mbsl-core yielded many such obligately aerobic isolates belonging to Cereibacter, Guyparkeria, Halomonas, Methylophaga, Pseudomonas and Sulfitobacter which died upon anaerobic incubation, despite being provided with all possible electron acceptors and fermentative substrates. High percentages of metatranscriptomic reads from the 275 cmbsf sediment-sample, and metagenomic reads from all 25 sediment-samples, matched the isolates' genomic sequences including those for aerobic metabolisms, genetic/environmental information processing and cell division, thereby illustrating the bacteria's in-situ activity, and ubiquity across the sediment-horizons, respectively. The findings hold critical implications for organic carbon sequestration/remineralization, and inorganic compounds oxidation, within the sediment realm of global marine OMZs.
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Project description:Fluorescence in situ hybridization (FISH) and rRNA slot blot hybridization with 16S rRNA-targeted oligonucleotide probes were used to investigate the phylogenetic composition of a marine Arctic sediment (Svalbard). FISH resulted in the detection of a large fraction of microbes living in the top 5 cm of the sediment. Up to 65.4% +/- 7.5% of total DAPI (4',6'-diamidino-2-phenylindole) cell counts hybridized to the bacterial probe EUB338, and up to 4.9% +/- 1.5% hybridized to the archaeal probe ARCH915. Besides delta-proteobacterial sulfate-reducing bacteria (up to 16% 52) members of the Cytophaga-Flavobacterium cluster were the most abundant group detected in this sediment, accounting for up to 12.8% of total DAPI cell counts and up to 6.1% of prokaryotic rRNA. Furthermore, members of the order Planctomycetales accounted for up to 3.9% of total cell counts. In accordance with previous studies, these findings support the hypothesis that these bacterial groups are not simply settling with organic matter from the pelagic zone but are indigenous to the anoxic zones of marine sediments. Members of the gamma-proteobacteria also constituted a significant fraction in this sediment (6.1% +/- 2.5% of total cell counts, 14.4% +/- 3.6% of prokaryotic rRNA). A new probe (GAM660) specific for sequences affiliated with free-living or endosymbiotic sulfur-oxidizing bacteria was developed. A significant number of cells was detected by this probe (2.1% +/- 0.7% of total DAPI cell counts, 13.2% +/- 4. 6% of prokaryotic rRNA), showing no clear zonation along the vertical profile. Gram-positive bacteria and the beta-proteobacteria were near the detection limit in all sediments.
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