Interspecies interactions between Pseudomonas protegens and Acinetobacter johnsonii shape the spoilage profile of Ostrea rivularis Gould.

Abstract

The occurrence of Pseudomonas protegens (PS) and Acinetobacter johnsoniii (AC) as key specific spoilage organisms (SSOs) in oyster spoilage is well recognized, yet their interspecies interactions and consequences for spoilage remain unclear. A sterile oyster mince model made by Ostrea rivularis Gould was used to compare the metabolic behavior of PS and AC under single- and co-culture during 4 °C storage by monitoring bacterial growth and total volatile basic nitrogen (TVB-N). Under co-culture, AC growth was significantly inhibited from mid-storage onward, whereas PS maintained a competitive advantage with only a minor, non-significant reduction. Accordingly, TVB-N accumulation in the co-culture group remained intermediate between the two single-cultures, indicating a non-additive spoilage outcome. Transcriptomics further revealed an asymmetric metabolic response. PS up-regulated pathways related to nutrient utilization, energy metabolism, and stress adaptation, consistent with an activated, resource-scavenging state. In contrast, AC exhibited widespread down-regulation of central metabolic functions and nutrient transport, while inducing genes associated with micro-aerobic respiration, sulfur reduction, and biofilm formation, suggesting a shift toward an energy-conserving survival mode under competitive pressure. Enhanced nutrient and oxygen consumption by PS may intensified resource limitation for AC, whereas AC metabolic remodeling may alter the local micro-environment and modulate the spoilage capacity of PS. These interactions reshape the spoilage profile of oyster mince, characterized by attenuated nitrogenous volatile accumulation and a potential shift toward sulfurous processes inferred from transcriptomics. Overall, the findings highlight how microbial competition and metabolic niche partitioning modulate oyster spoilage and provide mechanistic insights for interaction-targeted spoilage control strategies.