A unique porin meditates iron‐selective transport through cyanobacterial outer membranes

Abstract

Summary Cyanobacteria are globally important primary producers and nitrogen fixers with high iron demands. Low ambient dissolved iron concentrations in many aquatic environments mean that these organisms must maintain sufficient and selective transport of iron into the cell. However, the nature of iron transport pathways through the cyanobacterial outer membrane remains obscure. Here we present multiple lines of experimental evidence that collectively support the existence of a novel class of substrate‐selective iron porin, Slr1908, in the outer membrane of the cyanobacterium Synechocystis sp. PCC 6803. Elemental composition analysis and short‐term iron uptake assays with mutants in Slr1908 reveal that this protein is primarily involved in inorganic iron uptake and contributes less to the accumulation of other metals. Homologues of Slr1908 are widely distributed in both freshwater and marine cyanobacteria, most notably in unicellular marine diazotrophs. Complementary experiments with a homologue of Slr1908 in Synechococcus sp. PCC 7002 restored the phenotype of Synechocystis knockdown mutants, showing that this siderophore producing species also possesses a porin with a similar function in Fe transport. The involvement of a substrate‐selective porins in iron uptake may allow cyanobacteria to tightly control iron flux into the cell, particularly in environments where iron concentrations fluctuate.

The Role of Outer Membrane Protein(s) Harboring SLH/OprB-Domains in Extracellular Vesicles’ Production in Synechocystis sp. PCC 6803

“…On the other hand, cells transformed with pDC1841K showed no sign of complete chromosome segregation even after several rounds of streaking onto BG11 plates with increasing antibiotic concentration (Figure 2B). Our results are in agreement with the work of Qiu et al [19], in which the authors report to have failed in generating a full knockout mutant of gene slr1841. This suggests that Slr1841 likely plays an essential role in Synechocystis under the tested conditions, possibly involved in the uptake of micronutrients and/or in stabilizing the OM.…”

“…Growth phenotype characterization under photoautotrophic conditions in liquid medium indicated that none of the disrupted genes encode essential proteins for Synechocystis, at least under standard growth conditions, as all mutant strains showed similar growth rates as compared to that of the wild-type strain (Supplementary Material Figure S1). Qiu et al were also capable of generating full knockout mutants of genes sll1271, sll0772, slr0042 and sll1550, but not of slr1908 [19]. This discrepancy could be related to differences in Synechocystis sp.…”

“…This discrepancy could be related to differences in Synechocystis sp. PCC 6803 sub-strains used in the two different studies, and/or to the approach adopted for mutant generation (complete gene deletion in [19] vs. gene disruption by partial gene deletion in the present work).…”

Long‐term iron deprivation and subsequent recovery uncover heterogeneity in the response of cyanobacterial populations

“…3), we suggest that low‐fl Synechocystis 6803 cells lose their ability to recover after iron has been reintroduced into the medium. Studies have shown that the expression of iron uptake genes is upregulated under Fe‐limiting conditions (Singh et al ., 2003; Hernández‐Prieto et al ., 2012; Qiu et al ., 2018; Qiu et al ., 2021) and Fe transport rates in Synechocystis 6803 can increase by as much as 40‐fold compared with uptake rates in non‐limited cells (Kranzler et al ., 2011). This means that when iron bioavailability suddenly increases, high cellular uptake rates result in a surge of internal Fe quotas.…”

Comparative Phenotypic Analysis of Anabaena sp. PCC 7120 Mutants of Porinlike Genes

“…Recently it was described that in Synechocystis sp. the porin Slr1908 mediates the transport of inorganic iron [25]. Slr1908-like sequences were identified in many cyanobacterial species, indicating a porin-dependent iron uptake in cyanobacteria Nine porin-like genes were assigned based on sequence alignments and amino acid sequence properties in the genome of Anabaena sp.…”