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Coleman, O.I.* ; Sorbie, A.* ; Riva, A.* ; von Stern, M.* ; Kuhls, S.* ; Selegato, D.M.* ; Siegert, L.* ; Keidel, I.* ; Köhler, N.* ; Wirbel, J.* ; Kacprowski, T.* ; Dunkel, A.* ; Pauling, J.K.* ; Plagge, J.* ; Mediel-Cuadra, D. ; Wagner, S. ; Chadly, I.* ; Bierwith, S.* ; Peng, T. ; Metzler, T.* ; Li, X.* ; Heikenwälder, M.* ; Schafmayer, C.* ; Hinz, S.* ; Roder, C.* ; Röcken, C.* ; Zimmermann, M.* ; Rosenstiel, P.* ; Steiger, K.* ; Jesinghaus, M.* ; Liebisch, G.* ; Ecker, J.* ; Schmidt, C.* ; Zeller, G.* ; Janssen, K.P.* ; Haller, D.*

ATF6 activation alters colonic lipid metabolism causing tumour-associated microbial adaptation.

Nat. Metab. 7, 1830–1850 (2025)

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Endoplasmic reticulum unfolded protein responses contribute to cancer development, with activating transcription factor 6 (ATF6) involved in microbiota-dependent tumorigenesis. Here we show the clinical relevance of ATF6 in individuals with early-onset and late colorectal cancer, and link ATF6 signalling to changes in lipid metabolism and intestinal microbiota. Transcriptional analysis in intestinal epithelial cells of ATF6 transgenic mice (nATF6^IEC) identifies bacteria-specific changes in cellular metabolism enriched for fatty acid biosynthesis. Untargeted metabolomics and isotype labelling confirm ATF6-related enrichment of long-chain fatty acids in colonic tissue of humans, mice and organoids. FASN inhibition and microbiota transfer in germ-free nATF6^IEC mice confirm the causal involvement of ATF6-induced lipid alterations in tumorigenesis. The selective expansion of tumour-relevant microbial taxa, including Desulfovibrio fairfieldensis, is mechanistically linked to long-chain fatty acid exposure using bioorthogonal non-canonical amino acid tagging, and growth analysis of Desulfovibrio isolates. We postulate chronic ATF6 signalling to select for tumour-promoting microbiota by altering lipid metabolism.

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