Functional redundancy enables emergent metabolic dynamics in marine microbiomes

Abstract

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.