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Avian pathogenic  Escherichia coli  (APEC) is a facultative intracellular pathogen, and intracellular persistence in macrophages is essential for APEC extraintestinal dissemination. Until now, there is still no systematic interpretation of APEC intracellular proliferation. Intracellular survival factors, especially involved in pathometabolism, need to be further revealed. Acetate plays critical roles in supporting energy homeostasis and acts as a metabolic signal in the inflammatory response of eukaryotes. In this study, we identified that APEC  acs - yjcH - actP  operon, encoding acetate assimilation system, presented the host-induced transcription during its proliferation in macrophages. Our result showed that this acetate assimilation system acted as a novel intracellular survival factor to promote APEC replication within macrophages. Furthermore, deletion of  acs - yjcH - actP  operon in APEC decreased its cytotoxic level to macrophages. qRT-PCR results showed that the production of pro-inflammatory cytokines (IL-1β, IL-6, IL-8, IL-12β, and TNF-α) and iNOS in FY26∆ acs - yjcH - actP  infected macrophages were obviously down-regulated compared to that in wild-type FY26 infected cells. Deletion of  actP / yjcH / acs  genes attenuated APEC virulence and colonization capability in avian lungs in vivo for colibacillosis infection models. And acetate assimilation system acted as a virulence factor and conferred a fitness advantage during APEC early colonization. Taken together, our research unravelled the metabolic requirement of APEC intracellular survival/replication within macrophages, and acetate metabolic requirement acted as an important strategy of APEC pathometabolism. The intracellular acetate consumption during facultative intracellular bacteria replication within macrophages promoted immunomodulatory disorders, resulting in excessively pro-inflammatory responses of host macrophages.   Electronic supplementary material  The online version of this article (10.1186/s13567-019-0650-2) contains supplementary material, which is available to authorized users.

Acetate metabolic requirement of avian pathogenic Escherichia coli promotes its intracellular proliferation within macrophage