In March of 2020, the world entered lockdown and social distancing due to the onset of the COVID-19 pandemic. In the Martiny Lab of the Department of Earth System Sciences at the University of California Irvine, we watched as the latest lab-supported oceanographic research cruise was recalled from South Africa and instructed to steam directly back to the United States. Along with many others, we were left wondering how our lives, livelihoods, and careers would continue in the face of such unimaginable uncertainty. It was around this time that we received notice of the funding call for the 2021 U.S. Department of Energy Joint Genome Institute Community Science Program. Given the reprioritization of our collective time and efforts, this funding afforded us the amazing opportunity to embark on a long planned but unfulfilled goal to analyze over 10 years worth of microbial DNA data from a coastal time series at the Newport Pier in Newport Beach, California.   

The California coastal zone is a critical, mid-latitude eastern boundary upwelling system home to diverse species and commercially-valuable fisheries that are threatened by both warming and terrestrial inputs from 26.3 million coastal residents. In this system, El Niño acts as a natural analog for climate change impacts. However, little is known about in situ bacterial responses to anomalous warming and associated nutrient limitation in coastal environments. Thus, we proposed characterizing the biogeochemical role of nearshore bacteria from 2011-2020 in the Southern California Bight (SCB) at a long-term time series station that represents a nexus of monitoring efforts. During this time, SCB experienced a 2015 El Niño event and prolonged warming. 

The goals of this project were to (1) identify the metabolic adaptations of coastal bacterial populations to warming and changing nutrient availability and (2) link those changes to biogeochemistry at the terrestrial-aquatic interface in order to advance our understanding of how local anthropogenic nutrient loading, El Niño, and climatic changes affect microbial communities and marine ecosystems. As part of our proposal, we requested short-read, long-read, and single-cell sequencing. Roughly biweekly samples (2011 to 2020) from the “Microbes in the Coastal Region of Orange County” (MICRO) time series station were selected for short-read metagenomic sequencing. We also selected 4 pre-warming seasonal samples and 4 post-warming seasonal samples for long-read sequencing. Finally, we collected 4 seasonal samples over a year for single cell sequencing.

When our project was accepted for funding by JGI, a team of postdoctoral and graduate students embarked on a frosty month of -80C freezer diving in order to identify samples across the time series that were suitable for metagenomic sequencing.  Many pounds of dry ice and several rounds of quality control later, over 250 samples were identified as having high enough quality for analysis. These samples were sent to JGI for sequencing and bioinformatic processing. At the same time, students in the lab sequenced the latest DNA samples collected at MiCRO, then processed them using JGI’s bioinformatic pipeline available from NMDC EDGE. Finally, once all the data was compiled, we were able to begin our analysis of 10 years of microbial metagenomic data. 

In April of 2025, our article “Climate-driven succession in marine microbiome biodiversity and biogeochemical function” was published in Nature Communications. The analysis of short-read metagenomes from 267 time points (3.47 Tbp) over 10 years represents one of the longest metagenomic examinations of marine microbiomes to date and greatly enhances our ability to understand how long-term climate-driven changes impact marine communities. 

Our research shows seasonal and multi-annual cycles of temperature and inorganic nutrient supply influence parallel cycles of taxonomic and functional microbial biodiversity, suggesting compositionally and functionally dynamic ecosystems. We also find previously unrecognized changes in resource stress in heterotrophic bacteria that could be clearly tied to climate cycles and biogeochemistry. While much is understood about nutrient stress in phytoplankton, we know very little about heterotrophic bacteria. Specifically, we find genes associated with Fe stress tradeoff with genes associated with macronutrient (N and P) stress. This is seen over both seasonal and El Niño-Southern Oscillation cycles. Periods of high Fe stress were associated with cooler temperatures and high macronutrients during winter and La Niña conditions. In contrast, periods of high N and P stress were observed during warmer temperatures, summer months, and El Niño conditions. During warmer periods across multiple years, we also observed shifts to microbial communities with smaller genomes including Prochlorococcus and Pelagibacter, increased macronutrient stress genes, decreased organic carbon degradation potential, cells with high carbon-to-nutrient ratios, and low particulate organic carbon (POC) concentrations. These shifts are consistent with modeled projections of the impacts of anthropogenic climate change on marine ecosystems and suggest a strong, physicochemically-linked climate sensitivity of marine microbiome biodiversity and function. 

Overall, metagenomic analysis of over a decade of observations revealed that warming not only impacts microbial taxonomic composition, but results in large shifts in heterotrophic and autotrophic microbial gene content with strong linkages to marine iron, nitrogen, phosphorus, and carbon cycles. This work has clear implications for how microbial communities may respond to climate-driven warming in the future. Moreover, this work represents our first analysis of this novel JGI-supported dataset, with hopefully many more discoveries to come. 

For further information, you may access the full article at https://doi.org/10.1038/s41467-025-59382-1.