Spore formation in Clostridioides difficile is governed by small RNAs - an unexpected twist on the classic model of sporulation initiation. Clostridioides difficile produces highly resistant endospores that facilitate recovery after antibiotic treatment and host transmission. Spore formation is initiated by the master transcriptional regulator Spo0A, which triggers a hierarchical cascade of sigma factors that coordinate a transcriptional program resulting in spore formation. While the sporulation program is highly conserved in spore-forming Bacilli, the activation of Spo0A has remained unclear in many Clostridia, including C. difficile. Strict control of sporulation initiation, however, is essential because it inevitably results in the death of the mother cell. Using a suite of RNA-sequencing-based technologies, our lab has recently demonstrated that, in C. difficile, the Hfq chaperone binds and facilitates the regulatory activities of the majority of small RNAs in this gram-positive bacterium. We took advantage of this Hfq-dependence and performed an Hfq RIL-seq analysis in bacterial cultures undergoing sporulation to identify potential RNA regulators of spore formation. These analyses identified a plethora of sRNAs that base-pair with mRNAs encoding central regulators of spore formation, suggesting that they interfere with this morphogenic process at multiple stages. In particular, we identified a network of ten sRNAs that appear to regulate the initiation of sporulation directly via the spo0A mRNA. Our findings not only provide novel mechanistic insights into the control of sporulation initiation in C. difficile but also offer the opportunity to identify the environmental signals that regulate this process. Therefore, current research efforts focus on understanding how these sRNAs are integrated into transcriptional regulons. In the process, we identified the first example of a mixed regulatory circuit in C. difficile composed of the stress-response sigma factor SigB and a sigB-dependent sRNA that inhibits sporulation during acute infection-related stresses, such as oxygen exposure. Based on our data, we propose a stress-responsive mechanism in which a small RNA acts as a molecular switch, favoring a reversible stress response over irreversible differentiation into a spore.