An internal antisense RNA regulates expression of the photosynthesis gene isiA

Abstract

Small regulatory noncoding RNAs exist in both eukaryotic and prokaryotic organisms. Most of these RNA transcripts are transencoded RNAs with short and only partial antisense complementarity to their target RNAs, which regulate gene expression by modifying mRNA stability and translation. In contrast, reports on the function of cis-encoded, perfectly complementary antisense RNAs in eubacteria are rare. Cyanobacteria respond to iron deficiency by expressing IsiA (iron stress-induced protein A), which forms a giant ring structure around photosystem I. Here, we show that this process is controlled by IsrR (iron stress-repressed RNA), a cis-encoded antisense RNA transcribed from the isiA noncoding strand. Artificial overexpression of IsrR under iron stress causes a strongly diminished number of IsiA-photosystem I supercomplexes, whereas IsrR depletion results in premature expression of IsiA. The coupled degradation of IsrR͞isiA mRNA duplexes appears to be a reversible switch that can respond to environmental changes. IsrR is the only RNA known so far to regulate a photosynthesis component.cyanobacteria ͉ iron stress ͉ redox stress ͉ regulation of gene expression ͉ light harvesting

Good old-fashioned (anti)sense

“…Because cyanobacterial IsiR is complementary to the central region of the isiA message, a physical block of translation is unlikely to be involved. Rather, the pattern of appearance and disappearance of IsiR is consistent with a mechanism in which the duplexed RNAs are targeted for degradation (11). One mechanism of Hfq-ncRNA-mediated regulation in E. coli also seems to employ targeted degradation of a message, likely through RNaseE (9).…”

“…The observed effects on gene suppression were not, as expected, mediated by a physical block resulting from extensive base pairing with the target transcript: the active species are now recognized as highly processed 22-nt fragments that act in the context of an elaborate protein complex (10). In this issue of PNAS, Dühring et al (11) report a natural regulatory event in a cyanobacterium that comes close to the early expectations for straightforward antisense regulation: a 177-nt ncRNA is transcribed in antisense to the central portion of an iron-regulated transcript and blocks its accumulation, presumably through extensive base pairing.…”

“…Working with a cyanobacterial model organism for photosynthesis, Synechocystis sp. strain PCC 6803, Dühring et al (11) show that IsiR, an ncRNA complementary to the central portion of the isiA transcript, is regulated inversely with isiA (11). Overexpression or depletion of IsiR has the expected effects of suppressing or stimulating, respectively, the presence of isiA transcript and elaboration of the IsiA antenna around PSI (Fig.…”

“…The three conditions are interrelated in that both iron limitation and high light intensity indirectly cause oxidative stress (14). IsiR acts to regulate isiA expression in all three situations (11). Keeping isiA off in the absence of these stresses may be very important to the cell, because isiA can be very strongly induced, becoming the most abundant message after exposure to H 2 O 2 (16).…”

Non-coding RNAs in marine Synechococcus and their regulation under environmentally relevant stress conditions

“…Among the controlled processes is quorum sensing (Lenz et al, 2004;Tu et al, 2008Tu et al, , 2010Sonnleitner et al, 2011), the response to iron limitation (Wilderman et al, 2004;Masse et al, 2005), low temperature (Sledjeski et al, 1996), photosynthesis under iron limitation (Dü hring et al, 2006), pathogenicity and virulence (Lenz et al, 2004;Pfeiffer et al, 2007). Regulatory RNAs in prokaryotes are very diverse and can act through a multitude of different mechanisms (Hess and Marchfelder, 2011).…”