Microbially driven biogeochemical cycling of biogenic elements: processes, coupling mechanisms, and ecological implications

Microorganisms function as the fundamental architects and regulators of Earth’s biogeochemical cycles. Through their vast metabolic diversity, they govern the global fluxes and speciation of biogenic elements, including carbon (C), nitrogen (N), phosphorus (P), and sulfur (S), thereby exerting a profound influence on global climate dynamics, ecosystem stability, and environmental health. This review synthesizes current knowledge on the key microbial processes, their intricate interconnections, and their vulnerability and response to anthropogenic global change. We elucidate how microbial activities not only drive the individual cycles of these elements but also create a tightly woven network of coupled reactions that ultimately control the functioning of the biosphere. The carbon cycle is dynamically shaped by microbial activity. Heterotrophic decomposition of organic matter represents a primary source of atmospheric CO2, while the balance between methanogenesis, performed by archaea in anoxic environments, and methanotrophy, conducted by bacteria in oxic and anoxic zones, is critical for regulating the atmospheric burden of methane, a potent greenhouse gas. Conversely, photosynthetic and chemolithoautotrophic carbon fixation sequester inorganic carbon, with the Marine Microbial Carbon Pump (MCP) identified as a crucial mechanism for long-term carbon storage through the generation of recalcitrant dissolved organic carbon (RDOC). The nitrogen cycle, renowned for its complexity, involves multiple microbial guilds. Biological nitrogen fixation introduces reactive N into ecosystems, while nitrification and denitrification processes control its bioavailability and release nitrous oxide (N2O). The discovery of anaerobic ammonium oxidation (anammox) and complete ammonia oxidation (comammox) has revolutionized our understanding of nitrogen loss and efficiency, revealing shorter, more specialized pathways. In the phosphorus cycle, microbial solubilization of mineral phosphates and the orchestrated uptake/release of polyphosphates by polyphosphate-accumulating organisms (PAOs) directly modulate phosphorus bioavailability, a key determinant of primary productivity. Simultaneously, the sulfur cycle, driven by sulfate-reducing and sulfur-oxidizing prokaryotes, mediates redox transformations that are intimately linked to metal cycling and can lead to significant environmental acidification or alkalinization.A paradigm shift in biogeochemistry has been the recognition of extensive cross-element coupling. Metabolic strategies such as nitrate-dependent anaerobic methane oxidation (N-DAMO) directly link the carbon and nitrogen cycles, while sulfide-driven iron reduction connects sulfur and iron cycling, often leading to the mobilization of bound phosphorus. These interconnected pathways form robust, yet vulnerable, biogeochemical networks that enhance ecosystem functionality and resilience. However, these microbial engines are being fundamentally reshaped by global change. Climate warming, elevated CO2, nitrogen deposition, and pollution alter microbial community structure and metabolic rates. Warming accelerates soil respiration, potentially destabilizing vast carbon stocks, while permafrost thaw liberates ancient organic matter for microbial conversion into CO2 and CH4. Agricultural intensification homogenizes nitrifier communities, reducing nitrogen use efficiency and increasing N2O emissions. The expansion of oceanic oxygen-minimum zones promotes anaerobic processes like anammox, altering marine nitrogen budgets. While microbial communities possess a degree of resilience through functional redundancy and metabolic plasticity, there is a growing risk of exceeding critical thresholds or tipping points, such as the abrupt collapse of a permafrost carbon reservoir that could trigger irreversible feedbacks to the climate system.Looking forward, leveraging microbial processes is essential for developing sustainable solutions. Future research should integrate multi-omics technologies, cross-scale modeling, and synthetic biology to unravel complex microbial interactions and predict system-level responses. This knowledge is critical for harnessing microbial technologies such as anammox-based wastewater treatment, microbial carbon sequestration strategies, and next-generation biofertilizers to mitigate pollution, enhance agricultural sustainability, and achieve carbon neutrality goals. By bridging fundamental discovery with targeted engineering, we can unlock the immense potential of microorganisms to provide scientific support for achieving global sustainability objectives.