doi: 10.1038/s41467-022-28065-6.
Overlooked and widespread pennate diatom-diazotroph symbioses in the sea
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- PMID:35145076
- PMCID: PMC8831587
- DOI: 10.1038/s41467-022-28065-6
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Overlooked and widespread pennate diatom-diazotroph symbioses in the sea
Christopher R Schvarcz et al. Nat Commun..
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Abstract
Persistent nitrogen depletion in sunlit open ocean waters provides a favorable ecological niche for nitrogen-fixing (diazotrophic) cyanobacteria, some of which associate symbiotically with eukaryotic algae. All known marine examples of these symbioses have involved either centric diatom or haptophyte hosts. We report here the discovery and characterization of two distinct marine pennate diatom-diazotroph symbioses, which until now had only been observed in freshwater environments. Rhopalodiaceae diatoms Epithemia pelagica sp. nov. and Epithemia catenata sp. nov. were isolated repeatedly from the subtropical North Pacific Ocean, and analysis of sequence libraries reveals a global distribution. These symbioses likely escaped attention because the endosymbionts lack fluorescent photopigments, have nifH gene sequences similar to those of free-living unicellular cyanobacteria, and are lost in nitrogen-replete medium. Marine Rhopalodiaceae-diazotroph symbioses are a previously overlooked but widespread source of bioavailable nitrogen in marine habitats and provide new, easily cultured model organisms for the study of organelle evolution.
© 2022. The Author(s).
Conflict of interest statement
The authors declare no competing interests.
Figures
a,b,c Micrographs ofE. pelagica UHM3200 in valve view, including visualization bya scanning electron microscopy, and light microscopy forb live cells andc cells osmotically shocked to display the endosymbionts, as indicated by the black arrow. The osmotic shock treatment (c,f) disrupts host cell contents and displaces the endosymbionts. The natural intracellular location of endosymbionts is illustrated inn ando.d,e,f,g Micrographs ofE. catenata UHM3210 in girdle view, including visualization byd scanning electron microscopy, light microscopy fore live cells andf osmotically shocked cells with two endosymbionts highlighted by black arrowheads, andg undisturbed live cells growing in long chains. Micrographs ofEpSB (h,i,j) andEcSB (k,l,m) released from crushed UHM3200 and UHM3210 host cells, respectively, as seen under brightfield (h,k), phycoerythrin fluorescence (i,l), and chlorophyll fluorescence (j,m). Arrowheads point to the endosymbiont cells, and a singleSynechococcus WH7803 cell is present in each field to serve as a positive control for fluorescence.n,o Fluorescence micrographs of fixedE. pelagica andE. catenata cells, respectively, where endosymbionts (white arrows) and nuclei (red arrows) have been stained with nucleic acid-binding SYBR Gold dye (green). Inn, the fluorescence channel has been overlaid on a brightfield micrograph. Micrograph scale bars are 5 μm (a–c,n), 10 μm (d–f,o), 100 μm (g), and 3 μm (h–m). The experiment assessing the autofluorescence of released endosymbionts (h–m) was performed once, while all other micrographs represent results that were consistently reproduced in multiple experiments.
a Multigene phylogeny of theE. pelagica andE. catenata diatom hosts, based on the SSU (18S rRNA; 1322 nt),psbC (986 nt), andrbcL (1341 nt) genes.b Multigene phylogeny of theEpithemia endosymbionts, based on the SSU (16S rRNA; 420 nt) andnifH (760 nt) genes. The phylogenies are Bayesian majority consensus trees, and support values are provided for Bayesian and maximum likelihood methods (Bayesian posterior probabilities/ML bootstrap percent). Bold branches indicate complete support (posterior probability of 1 and bootstrap percent of 100), and the phylogeny scales are in units of nt substitutions per site. Labels for the new isolates (highlighted and bolded) include the dates and depths of collection. Accession numbers for all sequences are provided in the Source Data file.
Datasets screened include the Marine Atlas ofTara Oceans Unigenes (MATOU) and the representation of unigene MATOU-v1_93255274 inTara Oceans metagenomes and metatranscriptomes, as well asnifH amplicons published in NCBI’s non-redundant nucleotide (nt) and Sequence Read Archive (SRA) databases. Black dots indicate the location ofTara Oceans stations analyzed in MATOU. Source data are provided in the Source Data file.
a Dihydrogen (H2) production, ethylene (C2H4) production from acetylene (C2H2), and15N2 assimilation forE. pelagica UHM3200.b H2 production, C2H4 production from C2H2, and15N2 assimilation forE. catenata UHM3210. Sampling resolution was 10 min for H2 and C2H4 production and 2 h for the15N2 assimilation with the values represented by average ± standard deviation (n = 3). The15N2 assimilation beginning at 20:30 had rates of 0.1 fmol N cell−1 d−1 forE. pelagica. The night period is represented by gray shading in both plots. Source data are provided in the Source Data file.
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