Abstract
The Chlorophyll d-producing cyanobacterium Acaryochloris marina is widely distributed in marine environments enriched in far-red light, but our understanding of its genomic and functional diversity is limited. Here, we take an integrative approach to investigate A. marina diversity for 37 strains, which includes twelve newly isolated strains from previously unsampled locations in Europe and the Pacific Northwest of North America. A genome-wide phylogeny revealed both that closely related A. marina have migrated within geographic regions and that distantly related A. marina lineages can co-occur. The distribution of traits mapped onto the phylogeny provided evidence of a dynamic evolutionary history of gene gain and loss during A. marina diversification. Ancestral genes that were differentially retained or lost by strains include plasmid-encoded sodium-transporting ATPase and bidirectional NiFe-hydrogenase genes that may be involved in salt tolerance and redox balance under fermentative conditions, respectively. The acquisition of genes by horizontal transfer has also played an important role in the evolution of new functions, such as nitrogen fixation. Together, our results resolve examples in which genome content and ecotypic variation for nutrient metabolism and environmental tolerance have diversified during the evolutionary history of this unusual photosynthetic bacterium.
Highlights
The marine cyanobacterium Acaryochloris marina is unique in its use of Chlorophyll d (Chl d) as its major photosynthetic pigment [1]
Chl d is nearly identical in structure to the ubiquitous Chl a of other cyanobacteria, algae, and plants, this pigment absorbs strongly at far-red wavelengths that are inaccessible to most oxygenic phototrophs
For the salt tolerance experiment, each stock of growing cells was inoculated to an optical density at 750 nm (OD750 ) value of 0.01 in duplicate 125 mL flasks for each experimental salinity treatment (75 mL of ASN-III medium modified to contain final NaCl concentrations of 0, 0.2, 0.43, 0.5, 0.62, 0.8, or 1.6 M)
Summary
The marine cyanobacterium Acaryochloris marina is unique in its use of Chlorophyll d (Chl d) as its major photosynthetic pigment [1]. Chl d and its derivatives can be abundant in marine coastal ecosystems [3], and A. marina is widely distributed in temperate and tropical saline environments, often in association with red algae or animals [1,4–8] These cyanobacteria have been confirmed, through either laboratory cultivation or environmental DNA sequencing, to occur in marine stromatolites [9], a saline lake epilithic biofilm [10,11], a microbial mat from a high-elevation brackish lake [12], and the aquatic plant rhizosphere of a heavily canopied freshwater stream [13]. Improving our understanding of this variation is essential for inferring the different ways that this bacterium may contribute to ecosystem processes in far-red enriched environments We investigated this issue for our collection of 37 A. marina laboratory strains, including twelve newly isolated strains (Table S1). We identified differences among strains with respect to the presence of an intact CRISPR-Cas system, which may be selectively maintained when foreign DNA-induced mortality is high but otherwise lost
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