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 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 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 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.
Airborne bacteria and endotoxin may affect asthma and allergies. However, there is limited understanding of the environmental determinants that influence them. This study investigated the airborne ...microbiomes in the homes of 1038 participants from five cities in Northern Europe: Aarhus, Bergen, Reykjavik, Tartu, and Uppsala. Airborne dust particles were sampled with electrostatic dust fall collectors (EDCs) from the participants’ bedrooms. The dust washed from the EDCs’ clothes was used to extract DNA and endotoxin. The DNA extracts were used for quantitative polymerase chain (qPCR) measurement and 16S rRNA gene sequencing, while endotoxin was measured using the kinetic chromogenic limulus amoebocyte lysate (LAL) assay. The results showed that households in Tartu and Aarhus had a higher bacterial load and diversity than those in Bergen and Reykjavik, possibly due to elevated concentrations of outdoor bacterial taxa associated with low precipitation and high wind speeds. Bergen-Tartu had the highest difference (ANOSIM R = 0.203) in β diversity. Multivariate regression models showed that α diversity indices and bacterial and endotoxin loads were positively associated with the occupants’ age, number of occupants, cleaning frequency, presence of dogs, and age of the house. Further studies are needed to understand how meteorological factors influence the indoor bacterial community in light of climate change.
-related organisms comprise one of the most abundant deltaproteobacterial lineages in marine sediments where they occur throughout the sediment column in a gradient of increasing sulfate and organic ...carbon limitation with depth. Characterized
isolates are dissimilatory sulfate reducers able to grow by degrading aromatic hydrocarbons. The ecophysiology of environmental
-populations is poorly understood, however, possibly utilization of aromatic compounds may explain their predominance in marine subsurface sediments. We sequenced and analyzed seven
-related single-cell genomes (SAGs) from Aarhus Bay sediments to characterize their metabolic potential with regard to aromatic compound degradation and energy metabolism. The average genome assembly size was 1.3 Mbp and completeness estimates ranged between 20 and 50%. Five of the SAGs (group 1) originated from the sulfate-rich surface part of the sediment while two (group 2) originated from sulfate-depleted subsurface sediment. Based on 16S rRNA gene amplicon sequencing group 2 SAGs represent the more frequent types of
-populations in Aarhus Bay sediments. Genes indicative of aromatic compound degradation could be identified in both groups, but the two groups were metabolically distinct with regard to energy conservation. Group 1 SAGs carry a full set of genes for dissimilatory sulfate reduction, whereas the group 2 SAGs lacked any genetic evidence for sulfate reduction. The latter may be due to incompleteness of the SAGs, but as alternative energy metabolisms group 2 SAGs carry the genetic potential for growth by acetogenesis and fermentation. Group 1 SAGs encoded reductive dehalogenase genes, allowing them to access organohalides and possibly conserve energy by their reduction. Both groups possess sulfatases unlike their cultured relatives allowing them to utilize sulfate esters as source of organic carbon and sulfate. In conclusion, the uncultivated marine
populations are metabolically diverse, likely reflecting different strategies for coping with energy and sulfate limitation in the subsurface seabed.
Evaporative cooling towers to dissipate excess process heat are essential installations in a variety of industries. The constantly moist environment enables substantial microbial growth, causing both ...operative challenges (e.g., biocorrosion) as well as health risks due to the potential aerosolization of pathogens. Currently, bacterial levels are monitored using rather slow and infrequent sampling and cultivation approaches. In this study, we describe the use of metabolic activity, namely oxygen respiration, as an alternative measure of bacterial load within cooling tower waters. This method is based on optical oxygen sensors that enable an accurate measurement of oxygen consumption within a closed volume. We show that oxygen consumption correlates with currently used cultivation-based methods (R
= 0.9648). The limit of detection (LOD) for respiration-based bacterial quantification was found to be equal to 1.16 × 10
colony forming units (CFU)/mL. Contrary to the cultivation method, this approach enables faster assessment of the bacterial load with a measurement time of just 30 min compared to 48 h needed for cultivation-based measurements. Furthermore, this approach has the potential to be integrated and automated. Therefore, this method could contribute to more robust and reliable monitoring of bacterial contamination within cooling towers and subsequently increase operational stability and reduce health risks.
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.
Energy-starved microbes in deep marine sediments subsist at near-zero growth for thousands of years, yet the mechanisms for their subsistence are unknown because no model strains have been cultivated ...from most of these groups. We investigated Baltic Sea sediments with single-cell genomics, metabolomics, metatranscriptomics, and enzyme assays to identify possible subsistence mechanisms employed by uncultured
,
,
group OPB41,
,
,
,
,
, and
marine group II lineages. Some functions appeared to be shared by multiple lineages, such as trehalose production and NAD
-consuming deacetylation, both of which have been shown to increase cellular life spans in other organisms by stabilizing proteins and nucleic acids, respectively. Other possible subsistence mechanisms differed between lineages, possibly providing them different physiological niches. Enzyme assays and transcripts suggested that
and
group OPB41 catabolized sugars, whereas
and
catabolized peptides. Metabolite and transcript data suggested that
utilized allantoin, possibly as an energetic substrate or chemical protectant, and also possessed energy-efficient sodium pumps.
single-cell amplified genomes (SAGs) recruited transcripts for full pathways for the production of all 20 canonical amino acids, and the gene for amino acid exporter YddG was one of their most highly transcribed genes, suggesting that they may benefit from metabolic interdependence with other cells. Subsistence of uncultured phyla in deep subsurface sediments may occur through shared strategies of using chemical protectants for biomolecular stabilization, but also by differentiating into physiological niches and metabolic interdependencies.
Much of life on Earth exists in a very slow-growing state, with microbes from deeply buried marine sediments representing an extreme example. These environments are like natural laboratories that have run multi-thousand-year experiments that are impossible to perform in a laboratory. We borrowed some techniques that are commonly used in laboratory experiments and applied them to these natural samples to make hypotheses about how these microbes subsist for so long at low activity. We found that some methods for stabilizing proteins and nucleic acids might be used by many members of the community. We also found evidence for niche differentiation strategies, and possibly cross-feeding, suggesting that even though they are barely growing, complex ecological interactions continue to occur over ultralong timescales.
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