Gonzalez-Motos, S. | Search bioRxiv

bioRxiv2026

Decadal signatures of seasonal and ENSO-driven selection in microbial populations in distant oceans

Despite the crucial role of the ocean microbiome for global ecosystem processes, its response to global change remains poorly understood. Global change will exert selection on microbial species through changes in the genetic composition of their populations, favouring strains that are better adapted to new conditions. Analyzing long-term genomic variation in microbial populations inhabiting climatically comparable but oceanographically distinct regions may provide insights into their responses to future environmental conditions. We analyzed coastal marine microbiomes from two distant long-term observatories with Mediterranean-type climates but contrasting oceanographic regimes: the Blanes Bay Microbial Observatory (BBMO; Northwestern Mediterranean Sea) and the Microbes in the Coastal Region of Orange County (MiCRO; California coast, Pacific Ocean). Sampling conducted at least monthly during 15 and 10 years, respectively, yielded 1,535 Metagenome-Assembled Genomes (MAGs) in BBMO and 1,068 MAGs plus 187 Single-Amplified Genomes (SAGs) in MiCRO. Among these, we found 250 genomes with intraspecific (>95% genome similarity) representatives occurring at both sites. In contrast, at the strain-level threshold ([≥]99% genome similarity), only 13 BBMO genomes matched 15 closely related representatives in MiCRO. As genome similarity increased, we observed a shift from cosmopolitan to more coastal distributions and a slight increase in genome size, pointing to niche adaptation. Across both time series, we observed widespread seasonal population structure, with most genomes (~70%) showing significant seasonal structuring of variant composition. Moreover, in MiCRO, ~76% of the tested genomes also showed El Nino Southern Oscillation (ENSO)-associated structure in variant composition beyond seasonal effects. Focusing on a Prochlorococcus genome with intraspecific representatives at both locations (>96% genome similarity) we further found recurrent seasonal mutations and non-synonymous to synonymous mutation ratios (pN/pS) from multiple genes, together with signatures of positive selection (higher pN/pS) coinciding with El Nino events in MiCRO. This suggests an imprint of ENSO in marine microbial populations. Thus, beyond seasonality, long-term climatic oscillations may shape microbial populations. This has implications for understanding how the ocean microbiome will respond to long-term environmental change and prolonged disturbances through population-level genomic variation.

microbiology↗

bioRxiv2025

Functional redundancy enables emergent metabolic dynamics in marine microbiomes

Understanding how marine microbiomes will respond to ongoing global change is crucial. Functional redundancy, the capacity of different microbes to perform the same function, is considered a key mechanism underpinning the stability and resilience of the ocean microbiome. Although the extent of functional redundancy remains debated, investigating its manifestation in environmentally similar and interconnected microbial communities may provide critical insights into its role in shaping microbial community dynamics. We hypothesized that examining the long-term synchrony and rhythmicity of temperate microbial communities in such locations could provide insight into the role of functional redundancy. High functional redundancy at the community level would manifest as rhythmic and synchronous metabolic functions across sites, even in the absence of synchrony or rhythmicity at finer organizational levels, such as individual genes or taxa, thereby contributing to community resilience. Conversely, low functional redundancy would imply that synchrony and rhythmicity extend to both the contributing genes and taxa, suggesting a greater vulnerability of the community to environmental variability. To test this framework, we analyzed the long-term synchrony and rhythmicity of two marine-coastal microbiomes in the Mediterranean Sea, separated by approximately 150 km and connected by a dominant southwest current. Monthly collected metagenomes from a seven-year period were examined at the levels of metabolic functions (e.g., KEGG pathways), predicted genes (open reading frames), and taxa. We found functions, genes, and taxa exhibiting high, low, or anti-synchrony, as well as displaying rhythmic or non-rhythmic patterns. Although rhythmic behavior was observed on average across all organizational levels, consistent with the seasonal dynamics expected in temperate Mediterranean waters, average synchrony across microbiomes remained low. Focusing specifically on 45 markers of key biogeochemical functions, we revealed that several functions exhibited high synchrony and rhythmicity, in sharp contrast to the low synchrony and rhythmicity among the most abundant genes and taxa contributing to those functions. This suggests that functional redundancy and complementary dynamics at lower organizational levels, with distinct taxa contributing to key metabolic functions at different times, lead to rhythmic and synchronous dynamics at higher levels through emergent self-organization. Together, our results highlight functional redundancy and emergent self-organized dynamics as key mechanisms supporting the stability and resilience of marine microbiomes under environmental change.

ecology↗