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We report that the Gm7068 (CatSpere) and Tex40 (CatSperz) genes encode novel subunits of a 9-subunit CatSper ion channel complex. Targeted disruption of CatSperz reduces CatSper current and sperm rheotactic efficiency in mice, resulting in severe male subfertility. Normally distributed in linear quadrilateral nanodomains along the flagellum, the complex lacking CatSperζ is disrupted at ~0.8 μm intervals along the flagellum. This disruption renders the proximal flagellum inflexible and alters the 3D flagellar envelope, thus preventing sperm from reorienting against fluid flow in vitro and efficiently migrating in vivo. Ejaculated CatSperz-null sperm cells retrieved from the mated female uterus partially rescue in vitro fertilization (IVF) that failed with epididymal spermatozoa alone. Human CatSperε is quadrilaterally arranged along the flagella, similar to the CatSper complex in mouse sperm. We speculate that the newly identified CatSperζ subunit is a late evolutionary adaptation to maximize fertilization inside the mammalian female reproductive tract. DOI: http://dx.doi.org/10.7554/eLife.23082.001, eLife digest Male mammals ejaculate millions of sperm cells each time they mate with a female. Only a few of these cells manage to travel up the female’s reproductive tract to reach the egg, and usually only one sperm fertilizes it. Freshly ejaculated sperm are incapable of fertilizing eggs and have to undergo several changes within the female to become able to do so. One crucial change occurs in the sperm tail, which starts to beat vigorously in a whip-like motion. This type of movement – known as hyperactivated motility – enables the sperm to swim towards the egg, push through a sticky coating that surrounds it, and then burrow into it. Hyperactivated motility is triggered when calcium ions enter the sperm cell via a specific channel protein known as CatSper, which is found in the membrane that surrounds the cell. CatSper channels form groups (known as complexes) with several other proteins that are arranged in a unique pattern of four straight ‘stripes’ running down the tail of the sperm. This arrangement is necessary for hyperactivated motility and mutations in the genes that encode these proteins can lead to infertility in males. The CatSper channel complex is known to contain seven proteins: four that form a pore through which calcium ions can enter, and three accessory proteins whose roles in hyperactivated motility are less clear. Chung et al. identified two genes in mice that encode new accessory proteins in the CatSper channel complex named CatSper epsilon and CatSper zeta. Further experiments analyzed the role of CatSper zeta in more detail. Mutant males that lack CatSper zeta have fragmented patterns of CatSper stripes in the tails of their sperm. Moreover, fewer calcium ions were able to pass through the channels to enter the cell. Together, this made the sperm tail more rigid, which prevented it from moving efficiently within the female, resulting in reduced fertility. Chung et al. also found that the mutant sperm were less able to penetrate the egg than normal sperm. During evolution, the gene that encodes CatSper zeta appeared first in mammals and may represent an adaptation that improved the chances of a sperm fertilizing the egg inside the reproductive tract of female mammals. Future challenges will be to explore how the CatSper channel assembles on the membrane of sperm and find out exactly how calcium ions trigger hyperactivated motility. DOI: http://dx.doi.org/10.7554/eLife.23082.002

Spatial organization of the transcriptome has emerged as a powerful means for regulating the post-transcriptional fate of RNA in eukaryotes; however, whether prokaryotes use RNA spatial organization as a mechanism for post-transcriptional regulation remains unclear. Here we used super-resolution microscopy to image the E. coli transcriptome and observed a genome-wide spatial organization of RNA: mRNAs encoding inner-membrane proteins are enriched at the membrane, whereas mRNAs encoding outer-membrane, cytoplasmic and periplasmic proteins are distributed throughout the cytoplasm. Membrane enrichment is caused by co-translational insertion of signal peptides recognized by the signal-recognition particle. Time-resolved RNA-sequencing revealed that degradation rates of inner-membrane-protein mRNAs are on average greater that those of the other mRNAs and that this selective destabilization of inner-membrane-protein mRNAs is abolished by dissociating the RNA degradosome from the membrane. Together, these results demonstrate that the bacterial transcriptome is spatially organized and suggest that this organization shapes the post-transcriptional dynamics of mRNAs. DOI: http://dx.doi.org/10.7554/eLife.13065.001, eLife digest Within a cell, molecules of messenger RNA (mRNA) encode the proteins that the cell needs to survive and thrive. The amount of mRNA within a cell therefore plays an important role in determining both the amount and types of proteins that a cell contains and, thus, the behavior of the cell. In eukaryotic organisms, like humans, it has been established that it is not just the amount of mRNA that influences cell behavior, but also where the mRNA molecules are found within the cell. However, in bacteria, which are much smaller than human cells, it has long been believed that the location of an mRNA within the cell does not affect its behavior. Despite this, recent studies that have looked at small numbers of bacterial mRNAs have shown that some of these molecules are found in larger numbers than usual at certain sites inside cells. This suggests that location may actually affect the activity of some bacterial mRNAs. But do similar localization patterns occur for all of the thousands of different mRNAs that bacteria can make? To address this question, Moffitt et al. developed an approach that allows large, defined sets of mRNAs to be imaged in bacteria. Using this approach to study E. coli revealed that a considerable fraction of all the mRNAs that these bacteria can make locate themselves at specific sites within a cell. For example, mRNAs that encode proteins that reside inside the cell’s inner membrane are found enriched at this membrane. This localization also plays an important role in the life of these mRNAs, as they are degraded more quickly than those found elsewhere in the cell. This enhanced degradation rate arises partly because the enzymes that break down mRNA molecules are also found at the membrane. Thus, bacteria can shape the process by which an mRNA is made into protein by controlling where in a cell the mRNA is located. The next steps are to understand why bacteria use cell location to influence the rate of mRNA degradation. DOI: http://dx.doi.org/10.7554/eLife.13065.002