The “Dark Side” of Picocyanobacteria: Life as We Do Not Know It (Yet)

Abstract

Picocyanobacteria of the genus Synechococcus (together with Cyanobium and Prochlorococcus) have captured the attention of microbial ecologists since their description in the 1970s. These pico-sized microorganisms are ubiquitous in aquatic environments and are known to be some of the most ancient and adaptable primary producers. Yet, it was only recently, and thanks to developments in molecular biology and in the understanding of gene sequences and genomes, that we could shed light on the depth of the connection between their evolution and the history of life on the planet. Here, we briefly review the current understanding of these small prokaryotic cells, from their physiological features to their role and dynamics in different aquatic environments, focussing particularly on the still poorly understood ability of picocyanobacteria to adapt to dark conditions. While the recent discovery of Synechococcus strains able to survive in the deep Black Sea highlights how adaptable picocyanobacteria can be, it also raises more questions—showing how much we still do not know about microbial life. Using available information from brackish Black Sea strains able to perform and survive in dark (anoxic) conditions, we illustrate how adaptation to narrow ecological niches interacts with gene evolution and metabolic capacity.

Adaptive genetic traits in pelagic freshwater microbes

“…Metabolic analyses of MAGs and SAGs also boosted cultivation efforts by designing media based on metabolic traits (Lewis et al, 2021). Together with (semi‐)automated high‐throughput methods, they enabled the cultivation of several important microbial players of freshwater lakes (Callieri et al, 2022; Hahn & Hoetzinger, 2019; Henson et al, 2018; Kang et al, 2017; Kasalický et al, 2013; Neuenschwander et al, 2018; Salcher et al, 2015), whose physiology can now be studied in detail to analyse aspects not currently predictable by ‘omics’ methods. Moreover, whole‐genome sequencing of cultures is now state‐of‐the art for the description of new taxa and complete genomes from cultures allow to study metabolic traits, evolutionary history and (micro‐)diversification patterns in great detail (Cabello‐Yeves, Scanlan, et al, 2022; Cabello‐Yeves, Callieri, et al, 2022; Hahn, Burgsdorf, et al, 2021; Hahn, Huemer, et al, 2021; Hoetzinger & Hahn, 2017; Neuenschwander et al, 2018; Salcher et al, 2019).…”

“…Taking the order Synechococcales (order PCC‐6307 in GTDB, Figure 7D) as an example, which contains the most abundant and widespread aquatic picocyanobacteria (Cabello‐Yeves, Ghai, et al, 2017; Cabello‐Yeves, Haro‐Moreno, et al, 2017; Callieri, 2017; Callieri et al, 2022; Scanlan et al, 2009), we can discuss the nature of adaptation to marine versus freshwater habitats. Ancestral state reconstruction and phylogenetic analyses inferred that Synechococcales evolved from freshwater organisms (Cabello‐Yeves, Ghai, et al, 2017; Cabello‐Yeves, Haro‐Moreno, et al, 2017) that later transitioned into brackish and marine environments.…”

“…Ancestral state reconstruction and phylogenetic analyses inferred that Synechococcales evolved from freshwater organisms (Cabello‐Yeves, Ghai, et al, 2017; Cabello‐Yeves, Haro‐Moreno, et al, 2017) that later transitioned into brackish and marine environments. Three subclusters (SC) were established, whereof SC 5.1 contains mainly marine Synechococcus genomes (Synechococcus_C and Synechococcus_E in GTDB) and is ancestral to the dominant marine cyanobacterium Prochlorococcus (Callieri et al, 2022; Chisholm et al, 1988; Kashtan et al, 2014). The genera Cyanobium , Vulcanococcus and several unclassified Synechococcales (e.g.…”

Synthetic biology in marine cyanobacteria: Advances and challenges

“…Furthermore, considering their natural habitats where temperature, nutrient availability, salinity and light intensity constantly fluctuate, marine cyanobacteria are particularly robust to environmental changes (Ludwig and Bryant, 2012), which may be beneficial in an industrial context where growth parameters might vary slightly. While most species maintain a circadian rhythm, relying on complex regulatory cascades for adaptation to fluctuating light exposure, some species, isolated from light-deprived environments, show unique adaptability to growth in darkness (Coe et al, 2021;Callieri et al, 2022), further expanding their metabolic flexibility. In fact, the diversity of marine environments has been a driving force for cyanobacterial evolution and there is a high correlation between specialized features of some species and their natural habitats (Biller et al, 2015).…”

Ecophysiological analysis reveals distinct environmental preferences in closely related Baltic Sea picocyanobacteria

“…Sub‐cluster 5.3 includes both open ocean strains and a cosmopolitan group of freshwater strains (Cabello‐Yeves et al, 2017, 2018; Scanlan et al, 2009). Finally, the genetically diverse sub‐cluster 5.2 spans a wide range of salinity adaptations containing freshwater, brackish, and halotolerant strains (Cabello‐Yeves et al, 2018; Cabello‐Yeves, Callieri, et al, 2022; Cabello‐Yeves, Scanlan, et al, 2022; Callieri et al, 2021, 2022; Di Cesare et al, 2018; Sánchez‐Baracaldo et al, 2019) and contains a mix of strains assigned to Cyanobium spp. and Synechococcus spp.…”