Abstract
Microbially mediated carbon cycling is essential for the production of refractory dissolved organic carbon and subsequent formation of stable carbon sinks at the sediment–water interface (SWI) in aquatic ecosystems, such as lakes. It remains unclear how this process is influenced by hydrostatic pressure changes due to water level fluctuation in deep-water reservoirs. Here, a microcosm simulation experiment was carried out to decipher the response of microbially mediated carbon cycling to various hydrostatic pressures (i.e., 0.1 MPa [atmospheric pressure], 0.2 MPa, 0.5 MPa, 0.7 MPa) at the SWI in **pen Reservoir, Shaanxi Province, China. The response mechanisms of microbial community structure, functional gene abundance, and metabolic pathway activity associated with carbon cycling were explored by metagenomics and metabolomics. Results showed that the number of microbial species in sediment samples increased with elevating pressure. The relative abundance of archaea also increased from 0.2% to 0.4% as a consequence of pressure elevation, accompanied by 0.17% and 0.03% decrease in bacteria and fungi, respectively. In contrast with low pressures, high pressures allowed the microbial communities to form a more closely connected network, which maintained more complex interspecies interactions and greater system stability. High pressures additionally improved the abundances of specific functional genes (e.g., ALDO, ACO, sdhA, and sdhC) in carbon metabolic pathways, promoted carbon fixation by the reductive pentose phosphate (Calvin) and citrate cycles, and hindered methanogenesis. Piezophilic taxa (e.g., Gammaproteobacteria, Alphaproteobacteria, Bacteroidetes) and genes (e.g., ompH, asd) were identified among carbon cycling-associated microbial communities. The piezophilic genes, which were mainly present in the Proteobacteria phylum, increased first and then decreased in abundance with elevating pressure. The findings indicate that elevated hydrostatic pressure contributes to carbon sequestration at the SWI in deep-water reservoirs by changing carbon cycling-associated microbial species, as well as relevant functional genes and metabolic pathways.
Graphical Abstract
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Highlights
• Metagenomics and metabolomics unravel microbial mechanisms of C cycling at the sediment–water interface of reservoirs
• Distinct microbes contribute to C cycling, with improved community stability at high hydrostatic pressures
• Elevated pressure leads to enrichment of specific functional genes and metabolites in C fixation pathways
• Elevated pressure enhances the potential for microbially mediated C sequestration at the interface
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1 Introduction
The carbon cycle is one of the frontier topics in global change research, as there is still a tremendous challenge to achieve carbon neutrality by 2060 (Wang et al. 2023b). In addition to the effective control of anthropogenic emissions, searching for missing carbon sinks is the key to balancing the atmospheric CO2 budget (He et al. 2022). In this regard, the coupling of water and carbon cycles is a popular issue of carbon research (Guo et al. 2023).
Lakes and reservoirs receive a considerable amount of carbon from land surface water and may serve as carbon sources or sinks in the global carbon cycle (Deemer et al. 2016; Li et al. 2022b; Liu 2023; Soued et al. 2022). On the one hand, greenhouse gas emissions, such as CO2, CH4, and N2O, occur at the water–air interface of lakes and reservoirs. The CH4 emissions from reservoirs account for 12% of the global CH4 emissions (Ran et al. 2011). On the other hand, the surface sediments of lakes and reservoirs are important sites of carbon storage (Han et al. 2015). Under simulated experimental conditions, the abundance of bacteria, such as methanogens, decreased with increasing hydrostatic pressure (> 1.0 MPa) in river sediments upstream of a deep-water reservoir (Wu et al. 2021). Moreover, a higher hydrostatic pressure enhanced the expression of alkaline phosphatase-encoding genes (e.g., phoD, ppk, pqqC) and even promote phosphorus cycling at the SWI in a deep-water reservoir (Zhuo et al. 2021). Some researchers also demonstrated the influence of hydrostatic pressure on the composition, physiology, and metabolism of marine microbial communities (Wu et al. 2021). However, there has been insufficient research deciphering the mechanisms that allow hydrostatic pressure to influence microbial carbon cycling pathways at the SWI in large-scale deep-water reservoirs. This calls for research to unravel the response of microbial community structure, functional gene abundance, and metabolic pathway activity associated with carbon cycling to hydrostatic pressure changes at the SWI. The outcome will enable a mechanistic understanding of microbially mediated carbon migration and transformation in deep-water reservoirs, and lead to accurate assessment of carbon sequestration potential in reservoirs with different water depths.
Here, it was hypothesized that hydrostatic pressure could influence microbially mediated carbon cycling and drive carbon source/sink conversion at the SWI in deep-water reservoirs by altering associated microbial communities, functional genes, and metabolic pathways. To test the hypothesis, a microcosm experiment was conducted with hydrostatic pressure as the only variable, and four different pressures at the SWI were simulated using the sediment and water of a large drinking water reservoir. The changes in microbial species composition, functional gene abundance, and metabolic pathway activity associated with carbon cycling were investigated under different pressure levels. The results could offer novel insights into carbon source/sink conversion driven by microorganisms at the SWI in deep-water reservoirs and provide guidance for water level regulation during reservoir operation.
2 Materials and methods
2.1 Experimental setup and sampling
The sediment and water used in this study were collected from **pen Reservoir (34.057 N, 108.208 E; Fig. 1), which is located in ** ecotype diversification within Thaumarchaeota populations in the coastal ocean water column. ISME J 13(5):1144–1158. https://doi.org/10.1038/s41396-018-0311-x " href="/article/10.1007/s44246-024-00104-5#ref-CR31" id="ref-link-section-d146214046e1674">2019). Moreover, in the high-pressure group, microbial communities formed a larger network with more correlations, whereas the opposite result was obtained from the microbial network in the low-pressure group. Therefore, the microbial communities in surface waters may have intimate interactions among species and rapid response to external perturbations, with poor community stability; in contrast, the microbial communities in deep waters have a buffering effect on external perturbations, with relatively high community stability (Wang et al. 2022a).
Microorganisms whose growth and reproduction rates are optimized in high-pressure environments of the deep sea are known as piezophiles or barophiles (Peoples et al. 2019). The majority of piezophilic bacterial isolates are gram-negative bacteria, including the genera Shewanella and Psychromonas of the class Gammaproteobacteria, as well as some groups of the classes Deltaproteobacteria and Alphaproteobacteria. Compared with atmosphere pressure, higher pressures resulted in increased relative abundances of two genera in Gammaproteobacteria (i.e., Psychromonas, Shewanella), three genera in Alphaproteobacteria (i.e., Brevundimonas, Microvirga, Rhodopseudomonas), and the class Bacteroidetes, although their optimum hydrostatic pressure was slightly different (Fig. 7a). Some of the above-mentioned genera have been reported as piezophiles in the Mariana, Kermadec, and Yap Trenches (Peoples et al. 2019; Zhang et al. 2020). Due to the small pressure range used in the present study, there were indistinct changes in the relative abundance of piezophiles under various levels of hydrostatic pressure. Still, the results support that hydrostatic pressure can affect microbial species composition associated with carbon cycling at the SWI in deep-water reservoirs.
Piezophilic microorganisms and genes in reservoir sediments at various hydrostatic pressures. a Piezophiles with significant differences. b Numbers of phyla containing asd, ompH, and shared piezophilic genes. c Species that harbored the piezophilic genes with significant differences. d Abundance of the piezophilic genes. e Microbial metabolites associated with carbon cycling
To adapt to high-pressure environments, deep-sea microorganisms can evolve unique genes that are controlled by pressure. Some genes from barotolerant bacteria, such as ompH and asd, were not expressed when cloned into bacteria living in the atmosphere (Li et al. 2013). These two piezophilic genes were annotated in the present study, which exhibited similar trends in reservoir sediments at various hydrostatic pressures. Both ompH and asd were detected at the highest abundance in TU and FU groups, with the lowest in SU group. Notably, the absolute abundance of asd was higher than that of ompH (Fig. 7c), and was significantly different between FU and SU groups. Among the microbial communities associated with carbon cycling, there was a higher number of asd-harboring species than ompH-harboring species. Specifically, 146 species carried the asd gene only, 45 species contained the ompH gene only, and 22 species shared both genes. In total, the asd gene was detected in 19 phyla and the ompH gene in nine phyla, with the shared genes in six phyla (Fig. 7b). Among them, the phylum Proteobacteria comprised the largest number of species that contained the asd, ompH, and shared genes.
The species that harbored the asd, ompH, and shared genes with significant differences in abundance at various hydrostatic pressures are shown in Fig. 7d. The ompH gene abundance in Betaproteobacteria bacterium RIFCSPHIGHO2_12_FULL_69_13 was significantly higher at high pressures than at low pressures. The shared genes exhibited a similar trend to the ompH gene in some species of Proteobacteria (Deltaproteobacteria bacterium, uncultured Desulfatiglans sp.) and Candidatus (Rokubacteria bacterium). The abundance of most asd-harboring species trended upward from low to high hydrostatic pressure. Marietou and Bartlett (2014) et al. found that the relative abundances of α-Proteobacteria, γ-Proteobacteria, and Actinobacteria all increased with increasing hydrostatic pressure, possibly because piezophilic genes contributed to the formation of amino acids such as Asn, Cys, and Tyr (Zhao and **ao. 2017) for adaptation to the high-pressure environment. However, most of the previous studies on piezophilic microorganisms and genes have been conducted in seawater environments, where the piezophilic taxa are different from those found in reservoir sediments. For example, γ-Proteobacteria decreased in relative abundance with increasing hydrostatic pressure in the present study.
4.2 Hydrostatic pressure changes drive differences in carbon cycling-associated microbial functional genes and metabolic pathways
In the deep sea, only 1% of the organic matter used for ecosystem maintenance comes from the deposition of organic particulate matter on the ocean surface, and most of the organic matter is synthesized by deep-sea microorganisms using CO2 to provide nutrients (Wang et al. 2022b). Deep-sea autotrophic and facultative autotrophic microorganisms (e.g., ammonia-oxidizing archaea) absorb and utilize CO2 produced by heterotrophic microorganisms (e.g., Proteobacteria) to form the internal carbon cycle in the deep sea. These microorganisms also absorb a large amount of CO2 transported vertically to the seafloor from seawater. Therefore, the unique microbial communities in the deep-sea environment with high hydrostatic pressure play a positive role in the transformation and cycling of carbon, especially carbon sequestration. In deep-water reservoirs, although the hydrostatic pressure is not as high as that of the deep sea, there are still unique microbial communities containing piezophilic taxa and exhibiting specific functional characteristics. Moreover, deep-water reservoirs experience considerable water level fluctuations and unnatural flooding-drying habitat changes. The associated changes in water depth cause substantial variation in hydrostatic pressure, which could shape microbial communities and drive their structural and functional differences compared with those in the deep-sea environment. For example, the Three Gorges Reservoir is operated using a cyclic impoundment pattern; it impounds water in the winter and discharges water in the summer. The water level variation in front of the Three Gorges Dam is as high as 145–175 m (Pan et al. 2016), and the resulting changes in hydrostatic pressure would affect microbially mediated carbon sequestration at the SWI in the reservoir. In this regard, it is of theoretical and practical significance to decipher the influence of hydrostatic pressure changes on microbially mediated carbon cycling in deep-water reservoirs.
Based on the functional contribution of microbial species in carbon metabolic pathways (Fig. 4c), microorganisms as the major drivers and undertakers of carbon cycling participated in multiple CO2 fixation pathways at the SWI (Fig. 8). Among the major carbon-fixing groups, Candidatus Rokubacteria, Acidobacteria, Deltaproteobacteria, and Betaproteobacteria contributed up to 20% in the carbon fixation process. While microorganisms are both producers and consumers of methane, their metabolic processes are likely to be governed by environmental factors (e.g., pH) and soil nutrients (e.g., total N, P) (Wang et al. 2023a). In the present study, three microbial groups, Candidatus Rokubacteria, Deltaproteobacteria, and Acidobacteria, prominently contributed to methanogenesis and methane oxidation at the SWI. Candidatus Rokubacteria contributed the most to methanogenesis while having substantial contribution to methane oxidation. Additionally, Betaproteobacteria was the largest contributor to methane oxidation, with minimal contribution to methanogenesis. The total contribution of these four groups to methanogenesis and methane oxidation reached 30%, which decreased with elevating pressure. These carbon fixation, methanogenesis, and methane oxidation processes were also detected in the sediments of deep-sea cold seeps, where bacterial phyla such as Proteobacteria, Chloroflexi, and Acidobacteria played a key role in carbon metabolic pathways (Jiang et al. 2023). Taking into account the variation in the microbial contribution to carbon cycling pathways, the findings indicate that higher hydrostatic pressure could alter microbial community structure, thereby hindering methanogenesis and methane oxidation at the SWI.
With regard to the differential functional genes of carbon metabolism (Figs. 5, 8), there were considerable differences in carbon metabolic pathways at various hydrostatic pressures. The carbon fixation process involves the reductive pentose phosphate cycle (ALDO, rbcS, GAPDH), reductive citrate cycle (ACO, pycB, korA, sdhA, sdhC, fumB), and reductive acetyl–CoA pathway (metF, cdhD, cdhE). Among them, the ACO, pycB, and korA genes showed relatively high abundances, and multiple genes such as metF, ACO, sdhC, and sdhA had significant differences in response to changes in the hydrostatic pressure. ALDO, sdhA, sdhC, metF, and ACO gene abundances were increased by elevated pressures, in contrast to the downward trend in pycB, cdhD, and cdhE gene abundances. Wei et al. (2022) only annotated the ALDO and rbcS genes related to the Calvin cycle in surface sediments of the Mariana Trench. This means that microbially mediated carbon fixation pathways are slightly different between reservoir sediments and submarine trench sediments. Among the genes involved in methanogenesis (mch, mtrH, cdhE, cdhD), anaerobic oxidation of methane (mtrH), and aerobic oxidation of methane (mxaC), mch gene abundance was relatively high; mch and mxaC gene abundances exhibited an upward trend with elevating pressure, whereas cdhE and cdhD gene abundances displayed the opposite trend. Excluding cdhE and mxaC, these functional genes related to methane metabolism were also annotated in sediments of the Chao Lake (Zhou et al. 2023). Accordingly, reservoir sediments and lake sediments provide relatively similar habitat environments for microorganisms. With respect of the abundance of differential functional genes related to carbon metabolism, elevating the hydrostatic pressure promoted carbon fixation pathways—the reductive citrate and pentose phosphate cycles—at the SWI.
Furthermore, hydrostatic pressure had differential influence on the metabolites from various carbon cycling pathways (Fig. 7e). In the methanogenesis pathway, acetyl phosphate abundance was relatively high and increased with elevating pressure. The second and third most abundant metabolites were oxalacetic acid from the reductive citrate cycle and D-ribulose 5-phosphate from the reductive pentose phosphate cycle, respectively. The former decreased with increasing hydrostatic pressure, and the latter was most abundant in TU group. Other relatively abundant metabolites included succinic acid semialdehyde in the hydroxypropionate-hydroxybutylate cycle, as well as L-malic acid, succinic acid, and fumaric acid in the reductive citrate cycle. The three metabolites associated with the reductive citrate cycle all increased with increasing hydrostatic pressure. Recently, Shang et al. (2023) have found that microbially driven aerobic methane oxidation intercepts most of the CH4 in surface sediments of the Bohai Sea. As the intermediate products of methanogenesis and multiple carbon fixation pathways increased with elevating hydrostatic pressure, the present study indicates that higher hydrostatic pressure is conducive to reducing greenhouse gas emissions. The collective results suggest that microbially mediated carbon metabolism could enhance carbon sequestration potential at the SWI mainly by facilitating the reductive citrate and pentose phosphate cycles of carbon fixation and inhibiting methanogenesis.
5 Conclusions
Hydrostatic pressure is a major factor influencing the structural composition of sediment microbial communities. In this study, a simulation experiment was conducted with hydrostatic pressure as the only variable, corresponding to different water depths in a deep-water reservoir. Metagenomics and metabolomics were adopted to elaborate the response mechanisms of carbon cycling-associated microbial communities to pressure changes at the sediment–water interface (SWI) of the reservoir. The stability of sediment microbial communities was greater under high pressure conditions. The elevation in pressure contributed to the abundance of carbon-fixing bacteria such as Proteobacteria, Chloroflexi, and Actinobacteria, with piezophilic taxa and genes mainly found in the phylum Proteobacteria. Functional gene abundances of ALDO, ACO, sdhA, and sdhC increased in response to elevated pressure, along with the increase of metabolites from the reductive citrate and pentose phosphate (Calvin) cycles of carbon fixation and the accumulation of intermediate metabolites from the methanogenesis pathway to reduce methane production. The findings demonstrate that elevated hydrostatic pressure enhances carbon sequestration potential at the SWI of deep-water reservoirs by altering microbial community structure, functional gene abundance, and carbon metabolic pathways. This research provides insights into microbially mediated carbon cycling in deep-water reservoirs from a functional gene and metabolic pathway perspective. Future work is still needed to further explore related functional gene expression based on transcriptomic data, assess carbon sequestration by microbially mediated transformation of dissolved organic carbon from different sources to refractory organic carbon and refractory organic carbon production through the priming effect of fresh terrestrial organic carbon inputs at the SWI, as well as associated influencing factors and more explicit metabolic mechanisms of carbon transformation.
Availability of data and materials
The raw metagenomic reads reported in this paper have been deposited in the NCBI Sequence Read Archive (https://www.ncbi.nlm.nih.gov/) under BioProject accession number PRJNA815823.
Abbreviations
- RDOC:
-
Refractory dissolved organic carbon
- SWI:
-
Sediment–water interface
- AU:
-
Atmospheric pressure at 0.1 MPa
- TU:
-
0.2 MPa pressure
- FU:
-
0.5 MPa pressure
- SU:
-
0.7 MPa pressure
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This work was supported by the Science Fund for Distinguished Young Scholars of Hebei Province (grant No. E2022402064), the National Natural Science Foundation of China (grant Nos. U20A20316 and 72091511), and the Natural Science Foundation of Hebei Province (grant No. E2020402074).
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Writing–original draft, editing and visualization: [Yumei Li, Ying Pan]; Funding supporter: [Beibei Chai, Lixin He, **aohui Lei]; Investigation: [Kai Chen, Tianyu Zhuo]; Data analysis: [Yumei Li, Tianyu Zhuo, Kehong Yu]; Methodology: [Shilei Zhou]; Experimental design, review, editing and supervision: [Beibei, Chai]. All authors read and approved the final manuscript.
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Li, Y., He, L., Pan, Y. et al. Elevated hydrostatic pressure enhances the potential for microbially mediated carbon sequestration at the sediment–water interface in a deep-water reservoir by modulating functional genes and metabolic pathways. Carbon Res. 3, 19 (2024). https://doi.org/10.1007/s44246-024-00104-5
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DOI: https://doi.org/10.1007/s44246-024-00104-5