α-cyanobacteria possessing form IA RuBisCO globally dominate aquatic habitats

Abstract

RuBisCO (ribulose 1,5-bisphosphate carboxylase/oxygenase) is one the most abundant enzymes on Earth. Virtually all food webs depend on its activity to supply fixed carbon. In aerobic environments, RuBisCO struggles to distinguish efficiently between CO2 and O2. To compensate, organisms have evolved convergent solutions to concentrate CO2 around the active site. The genetic engineering of such inorganic carbon concentrating mechanisms (CCMs) into plants could help facilitate future global food security for humankind. In bacteria, the carboxysome represents one such CCM component, of which two independent forms exist: α and β. Cyanobacteria are important players in the planet’s carbon cycle and the vast majority of the phylum possess a β-carboxysome, including most cyanobacteria used as laboratory models. The exceptions are the exclusively marine Prochlorococcus and Synechococcus that numerically dominate open ocean systems. However, the reason why marine systems favor an α-form is currently unknown. Here, we report the genomes of 58 cyanobacteria, closely related to marine Synechococcus that were isolated from freshwater lakes across the globe. We find all these isolates possess α-carboxysomes accompanied by a form 1A RuBisCO. Moreover, we demonstrate α-cyanobacteria dominate freshwater lakes worldwide. Hence, the paradigm of a separation in carboxysome type across the salinity divide does not hold true, and instead the α-form dominates all aquatic systems. We thus question the relevance of β-cyanobacteria as models for aquatic systems at large and pose a hypothesis for the reason for the success of the α-form in nature.

Adaptive genetic traits in pelagic freshwater microbes

“…The most complex cyanobacterial genomes were recovered from soils, with genes involved in chemotaxis, membrane transport, motility and phototaxis ( pix gene cluster) being over‐represented in this group. These conclusions are further supported by a study comparing genomes of marine, brackish and freshwater isolates, that showed that both genome sizes (2.5 Mbp vs. 2.9 Mbp) and GC content (64% vs. 58.5%) were smaller in marine genomes compared to freshwater ones (Cabello‐Yeves, Callieri, et al, 2022; Cabello‐Yeves, Scanlan, et al, 2022). NiFe‐hydrogenases were among the genes that were enriched and could be responsible for adaptation to the pelagial of freshwaters, together with pyruvate ferredoxin oxidoreductase genes and the gas‐vesicle synthesis cluster ( gvpLFK ).…”

Elucidating the picocyanobacteria salinity divide through ecogenomics of new freshwater isolates

“…Given the phylogeny of the isolates obtained (see "Phylogeny of the new freshwater picocyanobacterial isolates" section below), this work only compares cluster 5 picocyanobacteria, specifically from the Synechococcus and Cyanobium genera, comprising isolates from different SCs (5.1, 5.2, 5.3) obtained from marine, brackish, and freshwater envionments. A parallel work compares cluster 5 picocyanobacteria (α-cyanobacteria) with other unicellular Synechococcus-like strains (β-cyanobacteria) [47]. We used only complete or near-complete genomes (draft) derived from cultures to reduce to a minimum the bias introduced from incomplete genomes derived from metagenomes (MAGs) and single cells (SAGs).…”

“…Being photoautotrophic, all genomes possessed a gene content consistent with their photosynthetic lifestyle, i.e., possessing photosystems I and II, NAD(P) H dehydrogenase, the cytochrome b6-f complex, ATP synthase, α-carboxysomes, type IA RuBisCOs (ribulose-1.5 biphosphate carboxylase-oxygenase) [47], and phycobilisomes (PBS) (Additional file 13: Table S6). We did note, however, some specific differences in some photosynthesis and light-harvesting genes.…”

“…All marine picocyanobacterial genomes used in this work were obtained from Cyanorak [28] as described recently [21]. We also used previously sequenced freshwater and brackish isolates [30,31,[33][34][35]92] together with our newly sequenced strains (see also [47]). Details of all the genomes used in this work and their genomic features, origin, and references are provided in Additional file 1: Table S1.…”

Acclimation of Nodularia spumigena CCY9414 to inorganic phosphate limitation – Identification of the P-limitation stimulon via RNA-seq

“…Bacteriocin synthesis clusters have not only been identified in the genomes of bloom-forming filamentous cyanobacteria, but are also present in the genomes of picocyanobacteria with smaller genomes, highlighting their importance for the organism because they are kept despite substantial genome reduction ( Paz-Yepes et al, 2013 ). Recently, it has been shown that such strains occur very frequently in the waters of different salinities including the Baltic Sea in summer ( Cabello-Yeves et al, 2022 ). Since most bloom formation associated genes, such as nitrogenase-related, gas-vesicle, bacteriocin and iron-acquisition genes, became more highly expressed only after 14 days under P-limiting conditions, we conclude that long-term harsh P-starvation can indeed be regarded as a potential trigger for bloom formation in Nodularia CCY9414 and likely other cyanobacteria.…”