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1. Nutrient-Colimited Trichodesmium as a Nitrogen Source or Sink in a Future Ocean

   https://doi.org/10.1128/AEM.02137-17  

   Walworth, Nathan G.; Fu, Fei-Xue; Lee, Michael D.; Cai, Xiaoni; Saito, Mak A.; Webb, Eric A.; Hutchins, David A.; Liu, Shuang-Jiang (February 2018, Applied and Environmental Microbiology)

   ABSTRACT Nitrogen-fixing (N 2 ) cyanobacteria provide bioavailable nitrogen to vast ocean regions but are in turn limited by iron (Fe) and/or phosphorus (P), which may force them to employ alternative nitrogen acquisition strategies. The adaptive responses of nitrogen fixers to global-change drivers under nutrient-limited conditions could profoundly alter the current ocean nitrogen and carbon cycles. Here, we show that the globally important N 2 fixer Trichodesmium fundamentally shifts nitrogen metabolism toward organic-nitrogen scavenging following long-term high-CO 2 adaptation under iron and/or phosphorus (co)limitation. Global shifts in transcripts and proteins under high-CO 2 /Fe-limited and/or P-limited conditions include decreases in the N 2 -fixing nitrogenase enzyme, coupled with major increases in enzymes that oxidize trimethylamine (TMA). TMA is an abundant, biogeochemically important organic nitrogen compound that supports rapid Trichodesmium growth while inhibiting N 2 fixation. In a future high-CO 2 ocean, this whole-cell energetic reallocation toward organic nitrogen scavenging and away from N 2 fixation may reduce new-nitrogen inputs by Trichodesmium while simultaneously depleting the scarce fixed-nitrogen supplies of nitrogen-limited open-ocean ecosystems. IMPORTANCE Trichodesmium is among the most biogeochemically significant microorganisms in the ocean, since it supplies up to 50% of the new nitrogen supporting open-ocean food webs. We used Trichodesmium cultures adapted to high-CO 2 conditions for 7 years, followed by additional exposure to iron and/or phosphorus (co)limitation. We show that “future ocean” conditions of high CO 2 and concurrent nutrient limitation(s) fundamentally shift nitrogen metabolism away from nitrogen fixation and instead toward upregulation of organic nitrogen-scavenging pathways. We show that the responses of Trichodesmium to projected future ocean conditions include decreases in the nitrogen-fixing nitrogenase enzymes coupled with major increases in enzymes that oxidize the abundant organic nitrogen source trimethylamine (TMA). Such a shift toward organic nitrogen uptake and away from nitrogen fixation may substantially reduce new-nitrogen inputs by Trichodesmium to the rest of the microbial community in the future high-CO 2 ocean, with potential global implications for ocean carbon and nitrogen cycling. 

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2. Alphaproteobacteria facilitate Trichodesmium community trimethylamine utilization

   https://doi.org/10.1111/1462-2920.15773  

   Conover, Asa_E; Morando, Michael; Zhao, Yiming; Semones, Jacob; Hutchins, David_A; Webb, Eric_A (October 2021, Environmental Microbiology)

   Summary In the surface waters of the warm oligotrophic ocean, filaments and aggregated colonies of the nitrogen (N)‐fixing cyanobacteriumTrichodesmiumcreate microscale nutrient‐rich oases. These hotspots fuel primary productivity and harbour a diverse consortium of heterotrophs. Interactions with associated microbiota can affect the physiology ofTrichodesmium, often in ways that have been predicted to support its growth. Recently, it was found that trimethylamine (TMA), a globally abundant organic N compound, inhibits N₂fixation in cultures ofTrichodesmiumwithout impairing growth rate, suggesting thatTrichodesmiumcan use TMA as an alternate N source. In this study,¹⁵N‐TMA DNA stable isotope probing (SIP) of aTrichodesmiumenrichment was employed to further investigate TMA metabolism and determine whether TMA‐N is incorporated directly or secondarily via cross‐feeding facilitated by microbial associates. Herein, we identify two members of the marineRoseobacterclade (MRC) of Alphaproteobacteria as the likely metabolizers of TMA and provide genomic evidence that they converted TMA into a more readily available form of N, e.g., ammonium (NH₄⁺), which was subsequently used byTrichodesmiumand the rest of the community. The results implicate microbiome‐mediated carbon (C) and N transformations in modulating N₂fixation and thus highlight the involvement of host‐associated heterotrophs in global biogeochemical cycling. 

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3. 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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4. Experimental assessment of tree canopy and leaf litter controls on the microbiome and nitrogen fixation rates of two boreal mosses

   https://doi.org/10.1111/nph.16611  

   Jean, Mélanie; Holland‐Moritz, Hannah; Melvin, April M.; Johnstone, Jill F.; Mack, Michelle C. (May 2020, New Phytologist)

   Summary Nitrogen (N₂)‐fixing moss microbial communities play key roles in nitrogen cycling of boreal forests. Forest type and leaf litter inputs regulate moss abundance, but how they control moss microbiomes and N₂‐fixation remains understudied. We examined the impacts of forest type and broadleaf litter on microbial community composition and N₂‐fixation rates ofHylocomium splendensandPleurozium schreberi.We conducted a moss transplant and leaf litter manipulation experiment at three sites with paired paper birch (Betula neoalaskana) and black spruce (Picea mariana) stands in Alaska. We characterized bacterial communities using marker gene sequencing, determined N₂‐fixation rates using stable isotopes (¹⁵N₂) and measured environmental covariates.Mosses native to and transplanted into spruce stands supported generally higher N₂‐fixation and distinct microbial communities compared to similar treatments in birch stands. High leaf litter inputs shifted microbial community composition for both moss species and reduced N₂‐fixation rates forH. splendens, which had the highest rates. N₂‐fixation was positively associated with several bacterial taxa, including cyanobacteria.The moss microbiome and environmental conditions controlled N₂‐fixation at the stand and transplant scales. Predicted shifts from spruce‐ to deciduous‐dominated stands will interact with the relative abundances of mosses supporting different microbiomes and N₂‐fixation rates, which could affect stand‐level N inputs. 

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5. Global phylogeography and microdiversity of the marine diazotrophic photoautotrophs Trichodesmium and UCYN-A

   https://doi.org/10.1128/msphere.00245-25  

   Nguyen, Angie; Ustick, Lucas J; Larkin, Alyse A; Martiny, Adam C (July 2025, mSphere)

   Campbell, Barbara J (Ed.)

   ABSTRACT Photoautotrophic diazotrophs, specifically the generaTrichodesmiumand UCYN-A, play a pivotal role in marine nitrogen cycling through their capacity for nitrogen fixation. Despite their global distribution, the microdiversity and environmental drivers of these diazotrophs remain underexplored. This study provides a comprehensive analysis of the global diversity and distribution ofTrichodesmiumand UCYN-A using the nitrogenase gene (nifH) as a genetic marker. We sequenced 954 samples from the Pacific, Atlantic, and Indian Oceans as part of the Bio-GO-SHIP project. Our results reveal significant phylogenetic and biogeographic differences between and within the two genera.Trichodesmiumexhibited greater microdiversity compared to UCYN-A, with clades showing region-specific distribution.Trichodesmiumclades were primarily influenced by temperature and nutrient availability. They were particularly frequent in regions of phosphorus stress. In contrast, UCYN-A was most frequently observed in regions experiencing iron stress. UCYN-A clades demonstrated more homogeneous distributions, with a single sequence variant within the UCYN-A1 clade dominating across varied environments. The biogeographic patterns and environmental correlations ofTrichodesmiumand UCYN-A highlight the role of microdiversity in their ecological adaptation and reflect their different ecological strategies. These findings underscore the importance of characterizing the global patterns of fine-scale genetic diversity to better understand the functional roles and distribution of marine nitrogen-fixing photoautotrophs.IMPORTANCEThis study provides insights into the global diversity and distribution of nitrogen-fixing photoautotrophs, specificallyTrichodesmiumand UCYN-A. We sequenced 954 oceanic samples of thenifHnitrogenase gene and uncovered significant differences in microdiversity and environmental associations between these genera.Trichodesmiumshowed high levels of sequence diversity and region-specific clades influenced by temperature and nutrient availability. In contrast, UCYN-A exhibited a more uniform distribution, thriving in iron-stressed regions. Quantifying these fine-scale genetic variations enhances our knowledge of their ecological roles and adaptations, emphasizing the need to characterize the genetic diversity of marine nitrogen-fixing prokaryotes. 

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