Proper regulation of germline gene expression is essential for fertility and maintaining species integrity. In the C. elegans germline, a diverse repertoire of regulatory pathways promote the expression of endogenous germline genes and limit the expression of deleterious transcripts to maintain genome homeostasis. TRIM-NHL proteins have emerged as conserved hubs of gene regulation across tissues and species, interfacing with multiple facets of RNA and protein regulatory pathways to ensure proper gene expression. Initially studied for its role in modulating miRISC activity via
let-7 and
lsy-6 in the soma, here we show that the conserved TRIM-NHL protein, NHL-2, plays an essential role in the C. elegans germline, modulating germline chromatin and meiotic chromosome organization. We show that NHL-2 localizes to germ granules, and uncover another role for NHL-2 in small RNA biology: as a co-factor in the biogenesis of both positively and negatively acting germline small RNA pathways (22G-RNAs). We show that NHL-2 physically and genetically interacts with the positively acting CSR-1 22G-RNA pathway, and our data support a model whereby NHL-2 is required for the activity of the RNA-dependent RNA Polymerase complex, which synthesizes 22G-RNAs. Furthermore, we demonstrate that NHL-2 is a bona fide RNA binding protein and, along with RNA-seq data from
nhl-2(
ok818) mutants, these results point to a small RNA-independent role for NHL-2 in regulating transcripts at the level of RNA stability. Collectively, our data implicate NHL-2 as an essential hub of gene regulatory activity in both the C. elegans germline and soma.