Small RNAs couple embryonic developmental programs to gut microbes

Maternal exposure to microbes and other environmental factors is known to induce adaptive changes in the progeny, but little is understood about how development of the progeny is changed. We show that Caenorhabditis elegans undergoes additional embryonic cell divisions in response to maternal gut microbes such as one producing the biopolymer {gamma}-poly-DL-glutamic acid. The divisions coincide with anatomical changes including left-right asymmetric cell alignment, doubling the association between intestinal cells and primordial germ cells, and improved fecundity. The developmental changes are regulated by soma-to-germline transmission of endogenous RNAi and the miR-35 microRNA family, which targets the LIN-23/CDC-25 pathway. Our findings challenge the widespread assumption that C. elegans has an invariant cell lineage that consists of 959 somatic cells and provide insights into how organisms optimize embryogenesis to adapt to environmental changes through epigenetic controls.