Open ocean and coastal strains of the N2-fixing cyanobacterium UCYN-A have distinct transcriptomes

Decades of research on marine N2 fixation focused on Trichodesmium, which are generally free-living cyanobacteria, but in recent years the endosymbiotic cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A) has received increasing attention. However, few studies have shed light on the infl...

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Published in:	PloS one 2023-05, Vol.18 (5), p.e0272674-e0272674
Main Authors:	Muñoz-Marín, María Del Carmen, Magasin, Jonathan D, Zehr, Jonathan P
Format:	Article
Language:	eng
Subjects:	Biogeochemical cycles Biology and Life Sciences Candidatus Atelocyanobacterium thalassa Cell division Chlorophyll Circadian rhythm Coastal environments Coastal waters Cyanobacteria Cyanobacteria - genetics Cyanobacteria - metabolism Earth Sciences Ecology and Environmental Sciences Genes Genomes Genomics Habitat changes Habitats Metabolism Metabolites Microorganisms Natural populations Nitrogen Nitrogen - metabolism Nitrogen fixation Nitrogen Fixation - genetics Nitrogenation Oceans Oceans and Seas Oxygen Physical Sciences Productivity Regulatory mechanisms (biology) Research and Analysis Methods Seawater Seawater - microbiology Symbiosis Transcriptome Transcriptomes Trichodesmium
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Summary:	Decades of research on marine N2 fixation focused on Trichodesmium, which are generally free-living cyanobacteria, but in recent years the endosymbiotic cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A) has received increasing attention. However, few studies have shed light on the influence of the host versus the habitat on UCYN-A N2 fixation and overall metabolism. Here we compared transcriptomes from natural populations of UCYN-A from oligotrophic open-ocean versus nutrient-rich coastal waters, using a microarray that targets the full genomes of UCYN-A1 and UCYN-A2 and known genes for UCYN-A3. We found that UCYN-A2, usually regarded as adapted to coastal environments, was transcriptionally very active in the open ocean and appeared to be less impacted by habitat change than UCYN-A1. Moreover, for genes with 24 h periodic expression we observed strong but inverse correlations among UCYN-A1, A2, and A3 to oxygen and chlorophyll, which suggests distinct host-symbiont relationships. Across habitats and sublineages, genes for N2 fixation and energy production had high transcript levels, and, intriguingly, were among the minority of genes that kept the same schedule of diel expression. This might indicate different regulatory mechanisms for genes that are critical to the symbiosis for the exchange of nitrogen for carbon from the host. Our results underscore the importance of N2 fixation in UCYN-A symbioses across habitats, with consequences for community interactions and global biogeochemical cycles.
ISSN:	1932-6203 1932-6203