The Anthropocene epoch is characterized by a dramatic increase in oil and steel production. In marine environments, the interaction between fuel and steel infrastructure leads to biodegradation of hydrocarbons and metal corrosion. Ballast tanks on naval ships, where seawater and diesel fuel intentionally mix, provide ideal microcosms for studying these processes. Since the 1960s, the US Navy has recognized corrosion problems linked to marine sulfate-reducing bacteria (SRB) in fuel storage tanks. Recent research has focused on understanding the biodegradability of various fuels, including biofuels, and their impact on corrosion. This study aimed to investigate the microbial communities and metabolic activities in the ballast tanks of Navy ships to determine the predominant mechanisms affecting diesel fuel fate and their relationship to infrastructure corrosion.

Existing literature highlights the corrosion issues in naval fuel tanks, often attributed to sulfate-reducing bacteria. Studies have investigated the biodegradability of various fuels under anaerobic conditions and the link between hydrocarbon oxidation and sulfide production. However, the in situ dynamics of microbial succession and their impact on corrosion in fuel-seawater mixtures remain unclear. This study builds upon previous work by examining the microbial community composition and metabolic processes within actual ship ballast tanks with varying residence times.

Ballast tank fluids were collected from three Navy vessels (Ships #1, #2, #3) with varying ballast residence times (1, ~20, and 31 weeks, respectively), along with a control vessel (Ship NF) without fuel-seawater mixing and San Diego harbor water. Samples were analyzed for dissolved oxygen, sulfate, and dissolved metals (Mn, Cu, Fe, Ni). Microbial populations were quantified using direct microscopy, qPCR, and metagenomic sequencing. Metagenomes were analyzed for community composition (16S rRNA gene sequencing) and functional genes involved in hydrocarbon degradation and electron transfer. Metabolite profiling (GC-MS) was performed to identify diagnostic intermediates in hydrocarbon degradation pathways. Suspended particles were analyzed using scanning electron microscopy with energy-dispersive X-ray analysis (EDX).

The San Diego Harbor water was dominated by *Alphaproteobacteria*, *Flavobacteria*, and *Gammaproteobacteria*, and marine eukaryotes. Ship #1 (1 week residence time) showed a significant shift towards *Gammaproteobacteria*, with enrichment of aerobic hydrocarbonoclastic taxa (*Marinobacter*, *Alcanivorax*, *Cycloclasticus*). Aerobic hydrocarbon degradation genes (*alkB*, *etbAa*, *tmoA*, *todC1*, *xylM*) and aerobic metabolites were abundant. Ship #2 (~20 weeks) showed an increase in *Deltaproteobacteria* (*Desulfuromonadales*), a decrease in aerobic hydrocarbon degradation genes, and a slight increase in anaerobic hydrocarbon activation genes (*nmsA*). Ship #3 (31 weeks) was dominated by anaerobic *Deltaproteobacteria* (*Desulfobacterales*, *Desulfarculales*, *Desulfovibrionales*), with a significant increase in sulfuroxyanion reduction genes and anaerobic hydrocarbon activation genes (*assA*, *bssA/hbsA/ibsA*, *nmsA*). Anaerobic metabolites (succinyl derivatives) were detected. All ballast tanks showed significantly higher concentrations of dissolved Mn, Cu, Fe, and Ni compared to harbor water, indicating biocorrosion. The relative abundance of metal sulfides correlated with the dominance of sulfidogenic taxa, particularly in Ship #3.

The findings reveal a clear successional pattern in microbial communities within the ballast tanks, driven by the availability of electron acceptors (oxygen, nitrate, sulfate). Initially, aerobic hydrocarbon degradation dominates, fueled by the readily available oxygen and hydrocarbons. As oxygen depletes, anaerobic bacteria, particularly sulfate-reducing *Deltaproteobacteria*, become dominant, utilizing sulfate as an electron acceptor. The production of sulfides likely contributes significantly to the corrosion observed in the ballast tanks. The shift from aerobic to anaerobic processes is further supported by the detected metabolites, which mirror the changes in the genetic potential encoded by the dominant taxa. This demonstrates the complex ecological dynamics between microbial activity, hydrocarbon biodegradation, and biocorrosion in marine systems.

This study demonstrates the rapid shift in microbial communities and metabolic activities within fuel-compensated ballast tanks, driving both hydrocarbon biodegradation and biocorrosion. Aerobic processes dominate early, followed by a transition to anaerobic degradation and sulfide production, leading to increased corrosion. These findings highlight the need for strategies to minimize microbial activity and mitigate the impact on ship infrastructure, such as preventing sediment introduction and employing protective coatings.

The study focused on a limited number of ships within the same class, and the inherent variability in operating practices and environmental conditions might affect generalizability. The sampling was restricted to expansion tanks, and the microbial communities in other parts of the ballast tank systems could differ. Further research is needed to fully elucidate the spatial heterogeneity within ballast tank systems and the precise mechanisms driving corrosion.