Escherichia coli contains a large CspA family, CspA to CspI. Here, we demonstrate that E. coli is highly protected against cold-shock stress, as these CspA homologues existed at approximately a total of two million molecules per cell at low temperature and growth defect was not observed until four csp genes (cspA, cspB, cspE and cspG) were deleted. The quadruple-deletion strain acquired cold sensitivity and formed filamentous cells at 15 degrees C although chromosomes were normally segregated. The cold-sensitivity and filamentation phenotypes were suppressed by all members of the CspA family except for CspD, which causes lethality upon overexpression. Interestingly, the cold sensitivity of the mutant was also suppressed by the S1 domain of polynucleotide phosphorylase (PNPase), which also folds into a beta-barrel structure similar to that of CspA. The present results show that cold-shock proteins and S1 domains share not only the tertiary structural similarity but also common functional properties, suggesting that these seemingly distinct protein categories may have evolved from a common primordial RNA-binding protein.