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1. Diurnal transcriptional variation is reduced in a nitrogen-fixing diatom endosymbiont

   https://doi.org/10.1093/ismejo/wrae064  

   Abresch, Heidi; Bell, Tisza; Miller, Scott_R (April 2024, The ISME Journal)

   Abstract Many organisms have formed symbiotic relationships with nitrogen (N)-fixing bacteria to overcome N limitation. Diatoms in the family Rhopalodiaceae host unicellular, N-fixing cyanobacterial endosymbionts called spheroid bodies (SBs). Although this relationship is relatively young, SBs share many key features with older endosymbionts, including coordinated cell division and genome reduction. Unlike free-living relatives that fix N exclusively at night, SBs fix N largely during the day; however, how SB metabolism is regulated and coordinated with the host is not yet understood. We compared four SB genomes, including those from two new host species (Rhopalodia gibba and Epithemia adnata), to build a genome-wide phylogeny which provides a better understanding of SB evolutionary origins. Contrary to models of endosymbiotic genome reduction, the SB chromosome is unusually stable for an endosymbiont genome, likely due to the early loss of all mobile elements. Transcriptomic data for the R. gibba SB and host organelles addressed whether and how the allocation of transcriptional resources depends on light and nitrogen availability. Although allocation to the SB was high under all conditions, relative expression of chloroplast photosynthesis genes increased in the absence of nitrate, but this pattern was suppressed by nitrate addition. SB expression of catabolism genes was generally greater during daytime rather than at night, although the magnitude of diurnal changes in expression was modest compared to free-living Cyanobacteria. We conclude that SB daytime catabolism likely supports N-fixation by linking the process to host photosynthetic carbon fixation. 

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2. Soil nitrogen fertilization reduces relative leaf nitrogen allocation to photosynthesis

   https://doi.org/10.1093/jxb/erad195  

   Waring, Elizabeth_F; Perkowski, Evan_A; Smith, Nicholas_G; Rogers, ed., Alistair (May 2023, Journal of Experimental Botany)

   Abstract The connection between soil nitrogen availability, leaf nitrogen, and photosynthetic capacity is not perfectly understood. Because these three components tend to be positively related over large spatial scales, some posit that soil nitrogen positively drives leaf nitrogen, which positively drives photosynthetic capacity. Alternatively, others posit that photosynthetic capacity is primarily driven by above-ground conditions. Here, we examined the physiological responses of a non-nitrogen-fixing plant (Gossypium hirsutum) and a nitrogen-fixing plant (Glycine max) in a fully factorial combination of light by soil nitrogen availability to help reconcile these competing hypotheses. Soil nitrogen stimulated leaf nitrogen in both species, but the relative proportion of leaf nitrogen used for photosynthetic processes was reduced under elevated soil nitrogen in all light availability treatments due to greater increases in leaf nitrogen content than chlorophyll and leaf biochemical process rates. Leaf nitrogen content and biochemical process rates in G. hirsutum were more responsive to changes in soil nitrogen than those in G. max, probably due to strong G. max investments in root nodulation under low soil nitrogen. Nonetheless, whole-plant growth was significantly enhanced by increased soil nitrogen in both species. Light availability consistently increased relative leaf nitrogen allocation to leaf photosynthesis and whole-plant growth, a pattern that was similar between species. These results suggest that the leaf nitrogen–photosynthesis relationship varies under different soil nitrogen levels and that these species preferentially allocated more nitrogen to plant growth and non-photosynthetic leaf processes, rather than photosynthesis, as soil nitrogen increased. 

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3. Endogenous clock-mediated regulation of intracellular oxygen dynamics is essential for diazotrophic growth of unicellular cyanobacteria

   https://doi.org/10.1038/s41467-024-48039-0  

   Bandyopadhyay, Anindita; Sengupta, Annesha; Elvitigala, Thanura; Pakrasi, Himadri B. (May 2024, Nature Communications)

   Abstract The discovery of nitrogen fixation in unicellular cyanobacteria provided the first clues for the existence of a circadian clock in prokaryotes. However, recalcitrance to genetic manipulation barred their use as model systems for deciphering the clock function. Here, we explore the circadian clock in the now genetically amenableCyanothece51142, a unicellular, nitrogen-fixing cyanobacterium. Unlike non-diazotrophic clock models,Cyanothece51142 exhibits conspicuous self-sustained rhythms in various discernable phenotypes, offering a platform to directly study the effects of the clock on the physiology of an organism. Deletion ofkaiA, an essential clock component in the cyanobacterial system, impacted the regulation of oxygen cycling and hindered nitrogenase activity. Our findings imply a role for the KaiA component of the clock in regulating the intracellular oxygen dynamics in unicellular diazotrophic cyanobacteria and suggest that its addition to the KaiBC clock was likely an adaptive strategy that ensured optimal nitrogen fixation as microbes evolved from an anaerobic to an aerobic atmosphere under nitrogen constraints. 

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4. Phosphoketolase and KDPG aldolase metabolisms modulate photosynthetic carbon yield in cyanobacteria

   https://doi.org/10.1093/plcell/koae291  

   Xie, Ningdong; Sharma, Chetna; Rusche, Katherine; Wang, Xin (December 2024, The Plant Cell)

   Abstract Cyanobacteria contribute to roughly a quarter of global net carbon fixation. During diel light/dark growth, dark respiration substantially lowers the overall photosynthetic carbon yield in cyanobacteria and other phototrophs. How respiratory pathways participate in carbon resource allocation at night to optimize dark survival and support daytime photosynthesis remains unclear. Here, using the cyanobacterium Synechococcus elongatus PCC 7942, we show that phosphoketolase integrates into a respiratory network in the dark to best allocate carbon resources for amino acid biosynthesis and to prepare for photosynthesis reinitiation upon photoinduction. Moreover, we show that the respiratory Entner–Doudoroff pathway in S. elongatus is incomplete, with its key enzyme 2-keto-3-deoxy-6-phosphogluconate aldolase exhibiting alternative oxaloacetate decarboxylation activity that modulates daytime photosynthesis. This activity allows for the bypassing of the tricarboxylic acid cycle when ATP and NADPH consumption for biosynthesis is excessive and imbalanced relative to their production by the light reactions, thereby preventing relative NADPH accumulation and ensuring optimal photosynthetic carbon yield. Optimizing these metabolic processes offers opportunities to enhance photosynthetic carbon yield in cyanobacteria and other photosynthetic organisms under diel light/dark cycles. 

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5. Defining the Sphagnum Core Microbiome across the North American Continent Reveals a Central Role for Diazotrophic Methanotrophs in the Nitrogen and Carbon Cycles of Boreal Peatland Ecosystems

   https://doi.org/10.1128/mbio.03714-21  

   Kolton, Max; Weston, David J.; Mayali, Xavier; Weber, Peter K.; McFarlane, Karis J.; Pett-Ridge, Jennifer; Somoza, Mark M.; Lietard, Jory; Glass, Jennifer B.; Lilleskov, Erik A.; et al (February 2022, mBio)

   Martiny, Jennifer B. (Ed.)

   ABSTRACT Peat mosses of the genus Sphagnum are ecosystem engineers that frequently predominate over photosynthetic production in boreal peatlands. Sphagnum spp. host diverse microbial communities capable of nitrogen fixation (diazotrophy) and methane oxidation (methanotrophy), thereby potentially supporting plant growth under severely nutrient-limited conditions. Moreover, diazotrophic methanotrophs represent a possible “missing link” between the carbon and nitrogen cycles, but the functional contributions of the Sphagnum -associated microbiome remain in question. A combination of metagenomics, metatranscriptomics, and dual-isotope incorporation assays was applied to investigate Sphagnum microbiome community composition across the North American continent and provide empirical evidence for diazotrophic methanotrophy in Sphagnum -dominated ecosystems. Remarkably consistent prokaryotic communities were detected in over 250 Sphagnum SSU rRNA libraries from peatlands across the United States (5 states, 17 bog/fen sites, 18 Sphagnum species), with 12 genera of the core microbiome comprising 60% of the relative microbial abundance. Additionally, nitrogenase ( nifH ) and SSU rRNA gene amplicon analysis revealed that nitrogen-fixing populations made up nearly 15% of the prokaryotic communities, predominated by Nostocales cyanobacteria and Rhizobiales methanotrophs. While cyanobacteria comprised the vast majority (>95%) of diazotrophs detected in amplicon and metagenome analyses, obligate methanotrophs of the genus Methyloferula (order Rhizobiales ) accounted for one-quarter of transcribed nifH genes. Furthermore, in dual-isotope tracer experiments, members of the Rhizobiales showed substantial incorporation of 13 CH 4 and 15 N 2 isotopes into their rRNA. Our study characterizes the core Sphagnum microbiome across large spatial scales and indicates that diazotrophic methanotrophs, here defined as obligate methanotrophs of the rare biosphere ( Methyloferula spp. of the Rhizobiales ) that also carry out diazotrophy, play a keystone role in coupling of the carbon and nitrogen cycles in nutrient-poor peatlands. IMPORTANCE Nitrogen availability frequently limits photosynthetic production in Sphagnum moss-dominated high-latitude peatlands, which are crucial carbon-sequestering ecosystems at risk to climate change effects. It has been previously suggested that microbial methane-fueled fixation of atmospheric nitrogen (N 2 ) may occur in these ecosystems, but this process and the organisms involved are largely uncharacterized. A combination of omics (DNA and RNA characterization) and dual-isotope incorporation approaches illuminated the functional diversity of Sphagnum -associated microbiomes and defined 12 bacterial genera in its core microbiome at the continental scale. Moreover, obligate diazotrophic methanotrophs showed high nitrogen fixation gene expression levels and incorporated a substantial amount of atmospheric nitrogen and methane-driven carbon into their biomass. Thus, these results point to a central role for members of the rare biosphere in Sphagnum microbiomes as keystone species that couple nitrogen fixation to methane oxidation in nutrient-poor peatlands. 

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