Transcriptomic and Proteomic Analysis Reveals Nitrogen Recycling as a Core Mechanism for Prochlorococcus Prolonged Survival

Abstract

Prochlorococcus, the dominant cyanobacterium in the oligotrophic ocean, possesses a streamlined genome and depends on interactions with heterotrophic bacteria for survival under various stressors. While the role of helper bacteria in mitigating oxidative stress is established, the mechanisms enabling its long-term survival under nitrogen (N) limitation remain poorly characterized. Here, we employ a multi-omics approach--integrating transcriptomics and proteomics--to investigate the physiological processes that facilitate the prolonged survival of Prochlorococcus in co-culture with the marine heterotroph Alteromonas during conditions of extreme N-deprivation. Our results demonstrate that, unlike axenic cultures which rapidly perish, Prochlorococcus in co-culture maintains viability for months following the depletion of initial N-sources. Molecular analysis identifies a shift in both organisms that underpins this persistence: Prochlorococcus strongly upregulates high-affinity N-scavenging pathways, while Alteromonas exhibits transcriptional and translational changes consistent with increased organic matter degradation and reduced motility. This suggests that Alteromonas functions as a key nitrogen recycler, providing a continuous, albeit low-level, supply of bioavailable NH4+ to its photoautotrophic partner through the remineralization of organic matter. These findings support and extend the Black Queen Hypothesis, illustrating that the benefits conferred by heterotrophs to genome-streamlined primary producers encompass not only the detoxification of reactive oxygen species but also the continuous provisioning of essential macro-nutrients under starvation conditions. This tightly coupled, mutualistic relationship represents a critical factor driving the resilience and productivity of microbial communities in oligotrophic marine ecosystems.