Microbial metabolism disrupts cytokine activity to impact host immune response

Proc Natl Acad Sci U S A. 2024 Nov 12;121(46):e2405719121. doi: 10.1073/pnas.2405719121. Epub 2024 Nov 8.

Abstract

Host-pathogen interactions are shaped by the metabolic status of both the host and pathogen. The host must regulate metabolism to fuel the immune response, while the pathogen must extract metabolic resources from the host to enable its own survival. In this study, we focus on the metabolic interactions of Mycobacterium abscessus with Drosophila melanogaster. We identify MAB_1132c as an asparagine transporter required for pathogenicity in M. abscessus. We show that this requirement is specifically associated with damage to the host: flies infected with MAB_1132c knockout bacteria, or with wild-type bacteria grown in asparagine-restricted conditions, are longer lived without showing a significant change in bacterial load. This is associated with a reduction in the host innate immune response, demonstrated by the decreased transcription of antimicrobial peptides as well as a significant reduction in the ability of the infection to disrupt systemic insulin signaling. Much of the increase in host survival during infection with asparagine-limited M. abscessus can be attributed to alterations in unpaired cytokine signaling. This demonstrates that asparagine transport in M. abscessus prior to infection is not required for replicative fitness in vivo but does significantly influence the interaction with the host immune responses.

Keywords: Drosophila melanogaster; Mycobacterium abscessus; infection; innate immunity; metabolism.

MeSH terms

  • Amino Acid Transport Systems / genetics
  • Amino Acid Transport Systems / metabolism
  • Animals
  • Asparagine / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cytokines* / metabolism
  • Drosophila melanogaster* / immunology
  • Drosophila melanogaster* / metabolism
  • Drosophila melanogaster* / microbiology
  • Host-Pathogen Interactions* / immunology
  • Immunity, Innate
  • Mycobacterium Infections, Nontuberculous / immunology
  • Mycobacterium Infections, Nontuberculous / metabolism
  • Mycobacterium Infections, Nontuberculous / microbiology
  • Mycobacterium abscessus* / immunology
  • Mycobacterium abscessus* / metabolism
  • Signal Transduction

Substances

  • Cytokines
  • Asparagine
  • Amino Acid Transport Systems
  • Bacterial Proteins