Climate change is causing increased ocean temperatures, particularly in coastal areas. The impact on microbial communities and biogeochemical cycling is poorly understood. This study utilizes a unique natural laboratory: a Baltic Sea bay warmed for 50 years by a nuclear power plant's cooling water discharge. This provides a long-term, naturally fluctuating system for studying effects similar to RCP8.5 climate change predictions. The Baltic Sea, a large brackish water area, is already affected by eutrophication, leading to hypoxia. Increased temperatures exacerbate hypoxia by decreasing oxygen solubility and increasing microbial metabolic rates. Shallow coastal waters are particularly vulnerable to warming, leading to prolonged hypoxia. Microbes in marine sediments are crucial for organic matter mineralization, carbon removal, and nutrient recycling. Their response to climate change is critical, yet how these fluctuations amplify effects through coastal sediment food webs remains unclear. The heated bay, with temperatures elevated by ~10°C above ambient, offers a comparison to a non-impacted control bay, allowing investigation into potential future changes under global warming. The study aims to understand how 50 years of warming affects microbial community diversity and structure, influences microbial energy and nutrient cycling, causes phenological shifts, and the consequences for future climate change.

Existing literature highlights the detrimental effects of climate change on global oceans, including increased CO2 concentrations, acidification, altered salinity, stratification, deoxygenation, and sea-level rise. Ocean temperatures are predicted to increase, with European seas already showing a rise since 1860. Experimental warming studies predict biodiversity reductions, but these often lack the temporal scale of natural systems. The Baltic Sea provides a case study, already experiencing eutrophication and hypoxia expansion. Warming accelerates hypoxia by reducing oxygen solubility and increasing microbial metabolism. Shallow coastal waters are highly sensitive to these effects, with more rapid heat transfer to sediments and potential for extended seasonal hypoxia. Microbial communities in marine sediments are key players in carbon cycling and nutrient recycling, representing early responders to climate change. However, the cascading effects of climate change on these communities and the wider food web remain poorly understood.

Sampling was conducted in a heated Baltic Sea bay (receiving cooling water discharge from a nuclear power plant for 50 years) and a control bay in 2018-2019. Four sampling occasions were conducted, with three sampling locations per bay (nine samples per bay per sampling occasion). Geochemical parameters (n=9 per bay per sampling) were measured in situ and from sediment cores. 16S rRNA gene amplicon sequencing (n=9 per bay per sampling) and community RNA transcript sequencing (n=3 per bay per sampling) were performed. Analysis involved characterizing geochemical changes (oxygen, organic matter, electron acceptors), microbial community diversity (Shannon's H, evenness, Chao1), community structure (16S rRNA and RNA transcripts via canonical correspondence analysis (CCA) and principal component analysis (PCA)), and metabolic responses (metatranscriptomics analysis). Statistical analyses, including ANOVA, GLM, PERMANOVA, and DESeq2, were used to compare the heated and control bays. The dataset was checked for doubletons and outliers.

The heated bay was 5.1°C warmer on average than the control bay, with greater differences in colder months. Oxygen concentrations were lower in the heated bay, likely due to increased metabolic rates. Sediment organic matter content was significantly higher in the heated bay, possibly due to increased primary production and necromass from algal blooms. Anaerobic nitrate reduction was indicated by higher nitrite and lower nitrate concentrations in the heated bay. Sulfate reduction rates were higher, evidenced by lower sulfate concentrations, and a shallower sulfate reduction zone, indicating that this process is shifting closer to the sediment-water interface. Microbial diversity (Shannon's H and evenness) and richness (Chao1) were significantly higher in the heated bay. CCA revealed that temperature, depth, and location were primary drivers of microbial community differences between the bays. The heated bay showed an increased relative abundance of sulfate-reducing bacteria (Desulfoplanes, Desulfofustis, Desulfomicrobium) and sulfur-oxidizing bacteria (Thiobacillaceae, Chromatiaceae, Sulfurovaceae) throughout the year. Metatranscriptomic analysis revealed increased transcripts associated with sulfate reduction and methanogenesis in the heated bay. Higher transcripts for ATP synthase suggested increased energy production, consistent with higher metabolic rates. However, a large number of stress-related transcripts (e.g., chaperones, DNA repair proteins) were also found, indicating that communities hadn’t fully adapted to the warmer conditions and may have weakened resilience. Cyanobacteria showed year-round activity in the heated bay compared to seasonal blooms in the control bay, potentially leading to prolonged anoxia.

The findings demonstrate that long-term warming selects for altered microbial communities with increased diversity and altered metabolic activity in coastal sediments. The increased energy production observed in the heated bay appears to be offset by energy expenditure on stress response. The higher abundance of Cyanobacteria in the heated bay, and their potential for year-round activity, could contribute to more frequent and prolonged anoxic conditions in coastal areas. The shallower anaerobic zones suggest increased potential for the release of methane, a potent greenhouse gas, to the water column. These results highlight a potential negative feedback loop, whereby warming may amplify negative effects on coastal biogeochemical cycling.

This study, conducted in a natural environment with seasonal fluctuations, demonstrates that 50 years of warming alters coastal sediment microbial communities, leading to increased diversity, shifts in metabolic activity, and potential for amplified negative effects on coastal biogeochemical cycling. While increased energy production is observed, community resilience is weakened by stress. Future research should investigate the generality of these findings across different coastal sediments and explore the long-term consequences of these changes for coastal ecosystems.

Potential differences in nutrient inputs between the heated and control bays could influence the results. While radioactivity was monitored and deemed not to be a significant factor, it was impossible to completely rule out the effects of other environmental factors that differ between the bays. The study is limited to one specific geographic location; future work should investigate the responses of coastal sediment microbial communities in other thermally-altered regions worldwide to assess the generality of findings. The sampling depth in this study was limited to shallow sediments (0-1cm and 6cm for flux calculations). Further studies in various sediment depths are required to better address this.