The genome content of metazoan mtDNA is not limited to 37 genes. Besides additional genes and other unusual features, small non coding RNAs (sncRNA) transcribed by mtDNA have been also found, but their occurrence and role are poorly understood. Are mitochondria able to influence nuclear gene expression through these sncRNAs? We sequenced small RNA libraries from gonadal tissues and isolated mitochondria of Ruditapes philippinarum, a species characterized by the Doubly Uniparental Inheritance (DUI) of mitochondria. This clam has two highly different sex-linked mtDNAs, each inherited uniparentally: one through females (F-type) the other through males (M-type). Since males are heteroplasmic for both types, and females are homoplasmic for the F-type, DUI provides an internal control without using Rho 0 cells, at least for sncRNAs transcribed by the M-type. We identified several putative sncRNAs of mitochondrial origin and we predicted their targets in silico. The most transcribed sncRNA we found is also differentially expressed in males and females, and its predicted target is the 3' UTR of the Nuclear Receptor Subfamily 0, known to be involved in sex determination of many animals. Actually, a role of mitochondria in sex determination has been hypothesized in the DUI system. Furthermore this sncRNA is transcribed by a non-coding mtDNA region that can be folded in a stable stem-hairpin structure, which makes it a good candidate for functional studies. Many other sncRNAs of mitochondrial origin are likely to be discovered soon, and we here propose to name them ‘small mitochondrial highly transcribed RNAs’ (smithRNAs).