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Complex coupled metabolic and prokaryotic community responses to increasing temperatures in anaerobic marine sediments: critical temperatures and substrate changes - PubMed

Complex coupled metabolic and prokaryotic community responses to increasing temperatures in anaerobic marine sediments: critical temperatures and substrate changes

Erwan G Roussel et al. FEMS Microbiol Ecol. 2015 Aug.

Abstract

The impact of temperature (0-80°C) on anaerobic biogeochemical processes and prokaryotic communities in marine sediments (tidal flat) was investigated in slurries for up to 100 days. Temperature had a non-linear effect on biogeochemistry and prokaryotes with rapid changes over small temperature intervals. Some activities (e.g. methanogenesis) had multiple 'windows' within a large temperature range (∼10 to 80°C). Others, including acetate oxidation, had maximum activities within a temperature zone, which varied with electron acceptor [metal oxide (up to ∼34°C) and sulphate (up to ∼50°C)]. Substrates for sulphate reduction changed from predominantly acetate below, and H2 above, a 43°C critical temperature, along with changes in activation energies and types of sulphate-reducing Bacteria. Above ∼43°C, methylamine metabolism ceased with changes in methanogen types and increased acetate concentrations (>1 mM). Abundances of uncultured Archaea, characteristic of deep marine sediments (e.g. MBGD Euryarchaeota, 'Bathyarchaeota') changed, indicating their possible metabolic activity and temperature range. Bacterial cell numbers were consistently higher than archaeal cells and both decreased above ∼15°C. Substrate addition stimulated activities, widened some activity temperature ranges (methanogenesis) and increased bacterial (×10) more than archaeal cell numbers. Hence, additional organic matter input from climate-related eutrophication may amplify the impact of temperature increases on sedimentary biogeochemistry.

Keywords: acetogenesis; anaerobic processes; chemolithotrophic; chemoorganotrophic; methanogenesis; mineralisation; sediment; sulphate reduction; temperature.

© FEMS 2015.

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Figures

Graphical Abstract Figure.
Graphical Abstract Figure.

Temperature increases had a non-linear effect on biogeochemistry and prokaryotes in marine sediments, with rapid changes over small temperature intervals which are relevant to climate change and the deep biosphere.

Figure 1.
Figure 1.

Effect of temperature and incubation time on sediment slurries (∼45 μM H2). (a) Specific metabolic activities (very low metabolic rates are not shown). Yellow dashed lines show acetoclastic methanogenic rates when overlaid by other activities. Green dashed lines show rates of autotrophic acetogenesis. (b) Putative substrates for sulphate reduction. (c) Main metabolic substrates and products. Blue dashed lines represent methane concentrations when overlaid by other compounds. Red dashed lines represent sulphate concentrations. aAnnual average in situ temperature. bTemperature at which at least 50% of sulphate reduction was hydrogenotrophic.

Figure 2.
Figure 2.

Effect of temperature and incubation time on the main substrate and product concentrations in substrate-amended sediment slurries (acetate, methylamine, H2). (a) Methane and H2 concentrations. (b) Acetate and sulphate concentrations. (c) Methylamine concentrations (between 10 and 100 days) and rates of methylotrophic acetogenesis in substrate-unamended slurries (∼45 μM H2). aAnnual average in situ temperature. bTemperature at which at least 50% of sulphate reduction could have been hydrogenotrophic.

Figure 3.
Figure 3.

The effect of temperature and time (15 and 100 days) on Bacteria and Archaea cell numbers (16S rRNA gene copies) in unamended (a and b) and substrate amended (c and d) sediment slurries. Cell numbers were calculated from 16S rRNA gene copy numbers by using the average 16S rRNA gene copy number for each taxa (4.19 and 1.71 copies for Bacteria and Archaea, respectively) deduced using the rrnDB database (Stoddard et al. 2015). Standard deviations are plotted but are mostly within the size of the symbols.

Figure 4.
Figure 4.

The effect of temperature on 16S rRNA gene diversity (PCR-DGGE) in substrate-amended slurries incubated for 100 days at different temperatures. (a) Archaea and (b) Bacteria.

Figure 5.
Figure 5.

Maximum activity rates for studied metabolic processes at different temperatures in sediment slurries (H2 ∼45 μM). aAnnual average in situ temperature (Arrows indicate range between minimum and maximum in situ temperature). bTemperature at which at least 50% of sulphate removal was hydrogenotrophic.

Figure 6.
Figure 6.

(a) Effect of temperature and incubation time on the net carbon mineralization balance of sediment slurries (∼45 μM H2). Net carbon mineralization balance was calculated by applying the standardizing factor in Table S1 (Supporting Information) to each specific rate, and then summing these. (b) Effect of temperature and incubation time on carbon dioxide concentrations measured from the slurry headspace (left vertical axis) and on the average carbon dioxide concentrations (open circles and right vertical axis). aAnnual average in situ temperature (Arrow indicates maximum average in situ temperature). bTemperature of maximum mineralization rate. cTemperature at which at least 50% of sulphate reduction was hydrogenotrophic. dFactor of increase of mineralization rate.

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