The cyanobacterium Prochlorococcus has divergent light-harvesting antennae and may have evolved in a low-oxygen ocean

Abstract

Marine picocyanobacteria of the genus Prochlorococcus are the most abundant photosynthetic organisms in the modern ocean, where they exert a profound influence on elemental cycling and energy flow. The use of transmembrane chlorophyll complexes instead of phycobilisomes as light-harvesting antennae is considered a defining attribute of Prochlorococcus Its ecology and evolution are understood in terms of light, temperature, and nutrients. Here, we report single-cell genomic information on previously uncharacterized phylogenetic lineages of this genus from nutrient-rich anoxic waters of the eastern tropical North and South Pacific Ocean. The most basal lineages exhibit optical and genotypic properties of phycobilisome-containing cyanobacteria, indicating that the characteristic light-harvesting antenna of the group is not an ancestral attribute. Additionally, we found that all the indigenous lineages analyzed encode genes for pigment biosynthesis under oxygen-limited conditions, a trait shared with other freshwater and coastal marine cyanobacteria. Our findings thus suggest that Prochlorococcus diverged from other cyanobacteria under low-oxygen conditions before transitioning from phycobilisomes to transmembrane chlorophyll complexes and may have contributed to the oxidation of the ancient ocean.

Keywords: anoxia; cyanobacteria; genomics; microbiology; oceanography.

Fig. 1.

Representative biogeochemical and flow-cytometry profiles and phylogenetic tree of unicellular cyanobacteria with Prochlorococcus from AMZs. (A) Dissolved oxygen concentration (blue), in vivo chlorophyll a fluorescence in relative units (dark green), and Synechococcus-like (orange) and Prochlorococcus-like (light green) cell abundance at Station 6 in the AMZ of the ETNP (Table 1). The gray area corresponds to depths with <0.5 μmol ⋅ kg⁻¹ O₂. (B) Fluorescence versus light scatter cytograms (in relative units) of cyanobacteria-like particles in the secondary deep-chlorophyll maximum. The upper panel shows particles with red fluorescence, a proxy for chlorophyll a-containing cells, and the lower panel shows particles with orange fluorescence, a proxy for phycoerythrin-containing cells. (C) Maximum-likelihood tree determined by phylogenetic inference using 49 concatenated ribosomal proteins: Prochlorococcus (collapsed genomes of recognized ecotypes in green), Synechococcus (collapsed genomes of marine subclusters in orange), and AMZ Prochlorococcus (in bold). PCC 7002 is the marine onshore Synechococcus sp. strain PCC 7002, and PCC 6803 is the freshwater Synechosystis sp. strain PCC 6803. The circles on each node represent support values higher than 50% (n = 1,000 iterations). Characteristic traits of the different cyanobacteria lineages examined are given in colored lines. The dashed line indicates that only a few members of the Synechococcus subcluster have that trait.

Fig. 2.

Presence–absence of selected genes in AMZ Prochlorococcus SAGs (see SI Appendix, Tables S2 and S3 for details).

Fig. 3.

Synteny and phylogeny of three genes involved in tetrapyrrole biosynthesis under oxygen-limited conditions. (A) Synteny of three orthologous genes involved in chlorophyll (acsF₂), phycocyanobilin (ho₂), and heme (hemN₂) biosynthesis across selected cyanobacterial lineages. The gene arsR encodes a putative transcriptional regulator, and yjbL encodes an unknown protein. Maximum-likelihood phylogenetic trees of (B) acsF-, (C) ho-, and (D) hemN-predicted amino acid sequences. The colored boxes mark the gene versions that appear organized in a cluster and should work under oxygen-limited conditions; lineages appearing in A are in bold. Conserved residues for several functions are given in SI Appendix, Fig. S6. Filled circles on each node correspond to support values higher than 50% (n = 1,000 iterations).