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.

Keywords: Black Sea; Synechococcus; mesopelagic zone; picocyanobacteria.

Figure 1

Protein-concatenated phylogenomic tree constructed with 371 core proteins with PhyloPhlAn3 tool. The tree includes all culture-derived picocyanobacteria from Synechococcus and Cyanobium genera inside sub-clusters 5.1, 5.2, and 5.3, a few Prochlorococcus representatives and Ca. Synechococcus spongiarum. The origin of each isolate is colour coded. The tree was rooted at the S. elongatus and PCC clade. Bootstrap values higher than 0.95 are marked as black squares on nodes. Modified from [26].

Figure 2

Typical structure of the envelope of a cyanobacterium (inspired from) [31,40,46].

Figure 3

Structure of the photosynthetic machinery in picocyanobacteria. The yellow arrows indicate the different wavelengths captured by phycobilisome (PBS) pigments and by chlorophyll a (Chl). The energy transfer can be carried out through spill-over from PSII (photosystem II) to PSI (photosystem I) or through state transition due to direct acquisition from PBS by PSI. AP (allophycocyanin), PC (phycocyanin), PE (phycoerythrin), Cyt b6f (cytochrome b6f).

Figure 4

Cultures of 17 freshwater strains of Synechococcus with different pigments that show the diversity in pigment composition with different pink, yellowish, and green colours (from [26], modified).

Figure 5

Vertical distribution of picocyanobacteria number in the West (St. 307) and East (JOSS-12) station of Black Sea (from [12,24], modified).

Figure 6

Cytograms of samples from different depths of the Black Sea (for methods, refer to [12]), (Cytometer Accuri C6, Becton Dickinson, Oxford, UK). In the density plots the pink dots are the picocyanobacteria. Orange fluorescence: FL2 channel = 585/40 nm and red fluorescence: FL3 channel >670 nm.

Figure 7

Picocyanobacteria from different depths (20, 30, 750, 1000 m), Black Sea, station 307, (epifluorescence microscopy, Zeiss Axioplan, 1250×, blue filters).