The Transcriptional Cycle Is Suited to Daytime N
            <sub>2</sub>
            Fixation in the Unicellular Cyanobacterium “
            <i>Candidatus</i>
            Atelocyanobacterium thalassa” (UCYN-A)

Muñoz-Marín, María del Carmen; Shilova, Irina N.; Shi, Tianshu; Farnelid, Hanna; Cabello, Ana María; Zehr, Jonathan P.

doi:10.1128/mbio.02495-18

Cited by 33 publications

(46 citation statements)

References 68 publications

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“…Here, we found evidence that Can. A. thalassa were active in summer in mid-shelf waters, while supporting the observations that, in contrast to other unicellular diazotrophic cyanobacteria, they fix N during the day (Muñoz-Marín et al, 2019).…”

Section: Resultssupporting

confidence: 84%

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

2020

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Environmental microbial gene expression patterns remain largely unexplored, particularly at interannual time scales. We analyzed the variability in the expression of marker genes involved in ecologically relevant biogeochemical processes at a temperate Atlantic site over two consecutive years. Most of nifH transcripts, involved in nitrogen (N) fixation, were affiliated with the symbiotic cyanobacterium Candidatus Atelocyanobacterium thalassa, suggesting a key role as N providers in this system. The expression of nifH and amoA (i.e., marker for ammonia oxidation) showed consistent maxima in summer and autumn, respectively, suggesting a temporal succession of these important N cycling processes. The patterns of expression of genes related to the oxidation of carbon monoxide (coxL) and reduced sulfur (soxB) were different from that of amoA, indicating alternate timings for these energy conservation strategies. We detected expression of alkaline phosphatases, induced under phosphorus limitation, in agreement with the reported co-limitation by this nutrient at the study site. In contrast, low-affinity phosphate membrane transporters (pit) typically expressed under phosphorus luxury conditions, were mainly detected in post-bloom conditions. Rhodobacteraceae dominated the expression of soxB, coxL and ureases, while Pelagibacteraceae dominated the expression of proteorhodopsins. Bacteroidetes and Gammaproteobacteria were major contributors to the uptake of inorganic nutrients (pit and amt transporters). Yet, in autumn, Thauma-and Euryarchaeota unexpectedly contributed importantly to the uptake of ammonia and phosphate, respectively. We provide new hints on the active players and potential dynamics of ecologically relevant functions in situ, highlighting the potential of metatranscriptomics to provide significant input to future omics-driven marine ecosystem assessment.

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Section: Resultssupporting

confidence: 84%

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

2020

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“…The cyanobacterial nitrogen fixation rhythm can be disconnected from light variations in laboratory experiments 23,52 , however genes related to this mechanism have yet to be fully understood. Our results echo previous work on the COP23 and Pex genes 53–56 , suggesting that at least some of these genes play a central role in the circadian rhythm of nitrogen fixation in T. erythraeum and T. thiebautii .…”

Section: Resultssupporting

confidence: 90%

Environmental genomics points to non-diazotrophic Trichodesmium species abundant and widespread in the open ocean

2021

Preprint

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Filamentous and colony-forming cells within the cyanobacterial genus Trichodesmium might account for nearly half of nitrogen fixation in the sunlit ocean, a critical mechanism that sustains plankton primary productivity at large-scale. Here, we report the genome-resolved metagenomic characterization of two newly identified marine species we tentatively named Ca. Trichodesmium miru and Ca. Trichodesmium nobis. Near-complete environmental genomes for those closely related candidate species revealed unexpected functional features including a lack of the entire nitrogen fixation gene apparatus and hydrogen recycling genes concomitant with the enrichment of nitrogen assimilation genes and apparent acquisition of the nirb gene from a non-cyanobacterial lineage. These comparative genomic insights were cross-validated by complementary metagenomic investigations. Our results contrast with the current paradigm that Trichodesmium species are necessarily capable of nitrogen fixation. The black queen hypothesis could explain gene loss linked to nitrogen fixation among Trichodesmium species, possibly triggered by gene acquisitions from the colony epibionts. Critically, the candidate species are not only widespread in the 3-2000 micron planktonic size fraction of the surface of the oceans and seas, but might also substantially expand the ecological niche of Trichodesmium, stressing the need to disconnect taxonomic signal for this genus from the ability of a microbial community to fix nitrogen. Especially, differentiating diazotrophic from non-diazotrophic populations when counting Trichodesmium filaments and colonies might help refine our understanding of the marine nitrogen balance. While culture representatives are needed to move beyond metagenomic insights, we are reminded that established links between taxonomic lineages and functional traits might not always hold true.

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“…Expression of genes involved in the cyt b 6 /f complex follow this same pattern. However, PSI genes were preferentially expressed at night, peaking at 22:00 h. Given the variability of the timing of PSI gene expression in N-fixing cyanobacteria (del Carmen Muñoz-Marin et al, 2019), and that degradation of PSI occurs during the night in Crocosphaera watsonii WH8501 (Masuda et al, 2018), nighttime expression of psa genes in Microcystis may be a genus-specific trait.…”

Section: Discussionmentioning

confidence: 99%

Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

et al. 2019

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This study examined diel shifts in metabolic functions of Microcystis spp. during a 48-h Lagrangian survey of a toxin-producing cyanobacterial bloom in western Lake Erie in the aftermath of the 2014 Toledo Water Crisis. Transcripts mapped to the genomes of recently sequenced lower Great Lakes Microcystis isolates showed distinct patterns of gene expression between samples collected across day (10:00 h, 16:00 h) and night (22:00 h, 04:00 h). Daytime transcripts were enriched in functions related to Photosystem II (e.g., psbA), nitrogen and phosphate acquisition, cell division (ftsHZ), heat shock response (dnaK, groEL), and uptake of inorganic carbon (rbc, bicA). Genes transcribed during nighttime included those involved in phycobilisome protein synthesis and Photosystem I core subunits. Hierarchical clustering and principal component analysis (PCA) showed a tightly clustered group of nighttime expressed genes, whereas daytime transcripts were separated from each other over the 48-h duration. Lack of uniform clustering within the daytime transcripts suggested that the partitioning of gene expression in Microcystis is dependent on both circadian regulation and physicochemical changes within the environment.

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The Transcriptional Cycle Is Suited to Daytime N ₂ Fixation in the Unicellular Cyanobacterium “ Candidatus Atelocyanobacterium thalassa” (UCYN-A)

Cited by 33 publications

References 68 publications

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

Environmental genomics points to non-diazotrophic Trichodesmium species abundant and widespread in the open ocean

Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

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The Transcriptional Cycle Is Suited to Daytime N 2 Fixation in the Unicellular Cyanobacterium “ Candidatus Atelocyanobacterium thalassa” (UCYN-A)

Cited by 33 publications

References 68 publications

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

Environmental genomics points to non-diazotrophic Trichodesmium species abundant and widespread in the open ocean

Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

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The Transcriptional Cycle Is Suited to Daytime N ₂ Fixation in the Unicellular Cyanobacterium “ Candidatus Atelocyanobacterium thalassa” (UCYN-A)