Slow Microbial Life in the Seabed Jørgensen, Bo Barker; Marshall, Ian P.G
Annual review of marine science,
01/2016, Letnik:
8, Številka:
1
Journal Article
Recenzirano
Global microbial cell numbers in the seabed exceed those in the overlying water column, yet these organisms receive less than 1% of the energy fixed as organic matter in the ocean. The microorganisms ...of this marine deep biosphere subsist as stable and diverse communities with extremely low energy availability. Growth is exceedingly slow, possibly regulated by virus-induced mortality, and the mean generation times are tens to thousands of years. Intermediate substrates such as acetate are maintained at low micromolar concentrations, yet their turnover time may be several hundred years. Owing to slow growth, a cell community may go through only 10,000 generations from the time it is buried beneath the mixed surface layer until it reaches a depth of tens of meters several million years later. We discuss the efficiency of the energy-conserving machinery of subsurface microorganisms and how they may minimize energy consumption through necessary maintenance, repair, and growth.
Cable bacteria of the Desulfobulbaceae family are centimeter-long filamentous bacteria, which are capable of conducting long-distance electron transfer. Currently, all cable bacteria are classified ...into two candidate genera: Candidatus Electronema, typically found in freshwater environments, and Candidatus Electrothrix, typically found in saltwater environments. This taxonomic framework is based on both 16S rRNA gene sequences and metagenome-assembled genome (MAG) phylogenies. However, most of the currently available MAGs are highly fragmented, incomplete, and thus likely miss key genes essential for deciphering the physiology of cable bacteria. Also, a closed, circular genome of cable bacteria has not been published yet. To address this, we performed Nanopore long-read and Illumina short-read shotgun sequencing of selected environmental samples and a single-strain enrichment of Ca. Electronema aureum. We recovered multiple cable bacteria MAGs, including two circular and one single-contig. Phylogenomic analysis, also confirmed by 16S rRNA gene-based phylogeny, classified one circular MAG and the single-contig MAG as novel species of cable bacteria, which we propose to name Ca. Electronema halotolerans and Ca. Electrothrix laxa, respectively. The Ca. Electronema halotolerans, despite belonging to the previously recognized freshwater genus of cable bacteria, was retrieved from brackish-water sediment. Metabolic predictions showed several adaptations to a high salinity environment, similar to the "saltwater" Ca. Electrothrix species, indicating how Ca. Electronema halotolerans may be the evolutionary link between marine and freshwater cable bacteria lineages.
Cable bacteria are centimeter-long filamentous bacteria that conduct electrons via internal wires, thus coupling sulfide oxidation in deeper, anoxic sediment with oxygen reduction in surface ...sediment. This activity induces geochemical changes in the sediment, and other bacterial groups appear to benefit from the electrical connection to oxygen. Here, we report that diverse bacteria swim in a tight flock around the anoxic part of oxygen-respiring cable bacteria and disperse immediately when the connection to oxygen is disrupted (by cutting the cable bacteria with a laser). Raman microscopy shows that flocking bacteria are more oxidized when closer to the cable bacteria, but physical contact seems to be rare and brief, which suggests potential transfer of electrons via unidentified soluble intermediates. Metagenomic analysis indicates that most of the flocking bacteria appear to be aerobes, including organotrophs, sulfide oxidizers, and possibly iron oxidizers, which might transfer electrons to cable bacteria for respiration. The association and close interaction with such diverse partners might explain how oxygen via cable bacteria can affect microbial communities and processes far into anoxic environments.
Recent work has shown that subsurface microbial communities assemble by selective survival of surface community members during sediment burial, but it remains unclear to what extent the compositions ...of the subsurface communities are a product of their founding population at the sediment surface or of the changing geochemical conditions during burial. Here we investigate this question for communities of sulfate-reducing microorganisms (SRMs). We collected marine sediment samples from the upper 3-5 m at four geochemically contrasting sites in the Skagerrak and Baltic Sea and measured SRM abundance (quantitative PCR of dsrB), metabolic activity (radiotracer rate measurements), and community composition (Illumina sequencing of dsrB amplicons). These data showed that SRM abundance, richness, and phylogenetic clustering as determined by the nearest taxon index peaked below the bioturbation zone and above the depth of sulfate depletion. Minimum cell-specific rates of sulfate reduction did not vary substantially between sites. SRM communities at different sites were best distinguished based on their composition of amplicon sequence variants (ASVs), while communities in different geochemical zones were best distinguished based on their composition of SRM families. This demonstrates environmental filtering of SRM communities in sediment while a site-specific fingerprint of the founding community is retained.
Cable bacteria are multicellular, filamentous bacteria that use internal conductive fibers to transfer electrons over centimeter distances from donors within anoxic sediment layers to oxygen at the ...surface. We extracted the fibers and used them as free‐standing bio‐based electrodes to investigate their electrocatalytic behavior. The fibers catalyzed the reversible interconversion of oxygen and water, and an electric current was running through the fibers even when the potential difference was generated solely by a gradient of oxygen concentration. Oxygen reduction as well as oxygen evolution were confirmed by optical measurements. Within living cable bacteria, oxygen reduction by direct electrocatalysis on the fibers and not by membrane‐bound proteins readily explains exceptionally high cell‐specific oxygen consumption rates observed in the oxic zone, while electrocatalytic water oxidation may provide oxygen to cells in the anoxic zone.
Biological cables as electrodes: Electrically conducting filamentous cable bacteria skeletons were used as free‐standing biological electrodes and displayed catalytic selectivity towards oxygen. The skeletons convert water to oxygen and oxygen back to water. We show that the reactions can be driven either by an external electric field or by simply exposing the cables to a gradient of oxygen concentration.
Studies have shown neighborhood walkability is associated with obesity. To advance this research, study designs involving longer follow-up, broader geographic regions, appropriate neighborhood ...characterization, assessment of exposure length and severity, and consideration of stayers and movers are needed. Using a cohort spanning the conterminous United States, this study examines the longitudinal relationship between a network buffer-derived, duration-weighted neighborhood walkability measure and two adiposity-related outcomes.
This study included 12,846 Black/African American and White adults in the REasons for Geographic And Racial Differences in Stroke study. Body mass index (BMI) and waist circumference (WC) were assessed at baseline and up to 13.3 years later (M (SD) = 9.4 (1.0) years). BMI and WC were dichotomized. Walk Score® was duration-weighted based on time at each address and categorized as Very Car-Dependent, Car-Dependent, Somewhat Walkable, Very Walkable, and Walker's Paradise. Unadjusted and adjusted logistic regression models tested each neighborhood walkability-adiposity association. Adjusted models controlled for demographics, health factors, neighborhood socioeconomic status, follow-up time, and either baseline BMI or baseline WC. Adjusted models also tested for interactions. Post-estimation Wald tests examined whether categorical variables had coefficients jointly equal to zero. Orthogonal polynomial contrasts tested for a linear trend in the neighborhood walkability-adiposity relationships.
The odds of being overweight/obese at follow-up were lower for residents with duration-weighted Walk Score® values in the Walker's Paradise range and residents with values in the Very Walkable range compared to residents with values in the Very Car-Dependent range. Residents with duration-weighted Walk Score® values classified as Very Walkable had significantly lower odds of having a moderate-to-high risk WC at follow-up relative to those in the Very Car-Dependent range. For both outcomes, the effects were small but meaningful. The negative linear trend was significant for BMI but not WC.
People with cumulative neighborhood walkability scores in the Walker's Paradise range were less likely to be overweight/obese independent of other factors, while people with scores in the Very Walkable range were less likely to be overweight/obese and less likely to have a moderate-to-high risk WC. Addressing neighborhood walkability is one approach to combating obesity.
Summary
The post‐glacial Baltic Sea has experienced extreme changes that are archived today in the deep sediments. IODP Expedition 347 retrieved cores down to 100 m depth and studied the climate ...history and the deep biosphere. We here review the biogeochemical and microbiological highlights and integrate these with other studies from the Baltic seabed. Cell numbers, endospore abundance and organic matter mineralization rates are extremely high. A 100‐fold drop in cell numbers with depth results from a small difference between growth and mortality in the ageing sediment. Evidence for growth derives from a D:L amino acid racemization model, while evidence for mortality derives from the abundance and potential activity of lytic viruses. The deep communities assemble at the bottom of the bioturbated zone from the founding surface community by selection of organisms suited for life under deep sediment conditions. The mean catabolic per‐cell rate of microorganisms drops steeply with depth to a life in slow‐motion, typical for the deep biosphere. The subsurface life under extreme energy limitation is facilitated by exploitation of recalcitrant substrates, by biochemical protection of nucleic acids and proteins and by repair mechanisms for random mismatches in DNA or damaged amino acids in proteins.
Summary
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.
See also the Commentary on this article by Cardini & Malkin, 232: 1897–1900.
Cable bacteria are electrically conductive, filamentous Desulfobulbaceae, which are morphologically, functionally, and phylogenetically distinct from the other members of this family. Cable bacteria ...have not been obtained in pure culture and were therefore previously described as candidate genera, Candidatus Electrothrix and Ca. Electronema; a representative of the latter is available as single-strain sediment enrichment. Here we present an improved workflow to obtain the first single-strain enrichments of Ca. Electrothrix and report their metagenome-assembled genomes (MAGs) and morphology. Based on these results and on previously published high-quality MAGs and morphological data of cable bacteria from both candidate genera, we propose to adopt the genus names Electrothrix and Electronema following the rules of the Code of Nomenclature of Prokaryotes Described from Sequence Data (SeqCode), with Electrothrix communis RBTS and Electronema aureum GSTS, respectively, as the nomenclatural types of the genera. Furthermore, based on average nucleotide identity (ANI) values < 95 % with any described species, we propose two of our three single-strain enrichment cultures as novel species of the genus Electrothrix, with the names E. aestuarii sp. nov. and E. rattekaaiensis sp. nov., according to the SeqCode.
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