skip to main content


Title: The cyanobacterium Prochlorococcus has divergent light-harvesting antennae and may have evolved in a low-oxygen ocean
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.  more » « less
Award ID(s):
1826734
NSF-PAR ID:
10325464
Author(s) / Creator(s):
; ; ; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
118
Issue:
11
ISSN:
0027-8424
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Angert, Esther (Ed.)
    Abstract

    Synechococcus cyanobacteria are ubiquitous and abundant in the marine environment and contribute to an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core, from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus cells to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examine the variability of gene content and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements for DNA integration and site-specific recombination, suggesting that their genomic variability relies in part on a “tycheposon”-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the core genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of incomplete lineage sorting in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.

     
    more » « less
  2. Despite very low concentrations of cobalt in marine waters, cyanobacteria in the genus Prochlorococcus retain the genetic machinery for the synthesis and use of cobalt-bearing cofactors (cobalamins) in their genomes. We explore cobalt metabolism in a Prochlorococcus isolate from the equatorial Pacific Ocean (strain MIT9215) through a series of growth experiments under iron- and cobalt-limiting conditions. Metal uptake rates, quantitative proteomic measurements of cobalamin-dependent enzymes, and theoretical calculations all indicate that Prochlorococcus MIT9215 can sustain growth with less than 50 cobalt atoms per cell, ∼100-fold lower than minimum iron requirements for these cells (∼5,100 atoms per cell). Quantitative descriptions of Prochlorococcus cobalt limitation are used to interpret the cobalt distribution in the equatorial Pacific Ocean, where surface concentrations are among the lowest measured globally but Prochlorococcus biomass is high. A low minimum cobalt quota ensures that other nutrients, notably iron, will be exhausted before cobalt can be fully depleted, helping to explain the persistence of cobalt-dependent metabolism in marine cyanobacteria. 
    more » « less
  3. Summary

    Synechococcus, a genus of unicellular cyanobacteria found throughout the global surface ocean, is a large driver of Earth's carbon cycle. Developing a better understanding of its diversity and distributions is an ongoing effort in biological oceanography. Here, we introduce 12 new draft genomes of marineSynechococcusisolates spanning five clades and utilize ~100 environmental metagenomes largely sourced from the TARA Oceans project to assess the global distributions of the genomic lineages they and other reference genomes represent. We show that five newly provided clade‐II isolates are by far the most representative of the recoveredin situpopulations (most ‘abundant’) and have biogeographic distributions distinct from previously available clade‐II references. Additionally, these isolates form a subclade possessing the smallest genomes yet identified of the genus (2.14 ± 0.05Mbps; mean ± 1SD) while concurrently hosting some of the highest GC contents (60.67 ± 0.16%). This is in direct opposition to the pattern inSynechococcus’s nearest relative,Prochlorococcus– wherein decreasing genome size has coincided with a strongdecreasein GC content – suggesting this new subclade ofSynechococcusappears to have convergently undergone genomic reduction relative to the rest of the genus, but along a fundamentally different evolutionary trajectory.

     
    more » « less
  4. Abstract

    Mixotrophic nanoflagellates can account for more than half of the bacterivory in the sunlit ocean, yet very little is known about their ecophysiology. Here, we characterize the grazing ecology of an open‐ocean mixotroph in the genusFlorenciella(class Dictyochophyceae). Members of this class were indirectly implicated as major consumers ofProchlorococcusandSynechococcusin the oligotrophic North Pacific Subtropical Gyre, but their phagotrophic capabilities have never been investigated. Our studies showed thatFlorenciellareadily consumedProchlorococcus,Synechococcus, and heterotrophic bacteria, and that the ingested prey relieved nutrient limitations on growth.Florenciellagrew faster (3 d−1) in nitrogen‐deplete medium given sufficient liveSynechococcus, than in nitrogen‐replete K medium (2 d−1), but it did not grow in continuous darkness. Grazing rates were substantially higher under nutrient limitation and showed a hint of diel variability, with rates tending to be highest near the end of the light period. An apparent trade‐off between the maximum clearance rate (5 nLFlorenciella−1h−1) and the maximum ingestion rate (up to ∼ 10 prey cellsFlorenciella−1h−1) across experiments suggests that grazing behavior may also vary in response to prey concentration. If the observed grazing rates are representative of other open‐ocean mixotrophs, their collective activity could account for a significant fraction of the daily cyanobacterial mortality. This study provides essential parameters for understanding the grazing ecology of a common marine mixotroph and the first characterization of mixotrophic nanoflagellate functional responses when feeding on unicellular cyanobacteria, the dominant marine primary producers in the oligotrophic ocean.

     
    more » « less
  5. null (Ed.)
    Synechococcus picocyanobacteria are ubiquitous and abundant photosynthetic organisms in the marine environment and contribute for an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon, based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examined the variability of gene sequences and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements including tyrosine recombinases, suggesting that their genomic plasticity relies on a tycheposon-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the rest of the genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of population-scale mechanisms in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events. 
    more » « less