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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Interactions between ultraviolet radiation exposure and phosphorus limitation in the marine nitrogen‐fixing cyanobacteria Trichodesmium and Crocosphaera
Increased stratification and mixed layer shoaling of the surface ocean resulting from warming can lead to exposure of marine dinitrogen (N2)‐fixing cyanobacteria to higher levels of inhibitory ultraviolet (UV) radiation. These same processes also reduce vertically advected supplies of the potentially limiting nutrient phosphorus (P) to N2fixers. It is currently unknown how UV inhibition and P limitation interact to affect the biogeochemical cycles of nitrogen and carbon in these biogeochemically critical microbes. We investigated the responses of the important and widespread marine N2‐fixing cyanobacteria
- NSF-PAR ID:
- 10457099
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Limnology and Oceanography
- Volume:
- 65
- Issue:
- 2
- ISSN:
- 0024-3590
- Page Range / eLocation ID:
- p. 363-376
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary In the surface waters of the warm oligotrophic ocean, filaments and aggregated colonies of the nitrogen (N)‐fixing cyanobacterium
Trichodesmium create 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 ofTrichodesmium without impairing growth rate, suggesting thatTrichodesmium can use TMA as an alternate N source. In this study,15N‐TMA DNA stable isotope probing (SIP) of aTrichodesmium enrichment 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 marineRoseobacter clade (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 byTrichodesmium and 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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Dinitrogen (N2) fixation is carried out by specialized microbes, called diazotrophs, and is a major source of nitrogen supporting primary production in oligotrophic oceans. One of the best-characterized diazotroph habitats is the North Pacific Subtropical Gyre (NPSG), where warm, chronically N-limited surface waters promote year-round N2fixation. At Station ALOHA (A Long-Term Oligotrophic Habitat Assessment) in the NPSG, N2fixation is typically ascribed to conspicuous, filamentous cyanobacterial diazotrophs (
Trichodesmium andRichelia ), unicellular free-livingCrocosphaera , and the UCYN-A/haptophyte symbiosis, based on using microscopy and quantitative PCR (qPCR). However, the diazotroph community in this ecosystem is diverse and includes non-cyanobacterial diazotrophs (NCDs). We investigated the diversity, depth distributions, and seasonality of diazotroph communities at Stn. ALOHA using high throughput sequencing (HTS) ofnifH gene fragments from samples collected throughout the euphotic zone (0-175 m) at near-monthly intervals from June 2013 to July 2016. The UCYN-A symbioses andTrichodesmium sp. consistently had the highest relative abundances and seasonal patterns that corroborated qPCR-based analyses. Other prevalent community members included a newCrocosphaera -like species, and several NCDs affiliated with γ- and δ-proteobacteria. Notably, some of the NCDs appear to be stable components of the community at Stn. ALOHA, having also been reported in prior studies. Depth and temporal patterns in microdiversity within two major diazotroph groups (Trichodesmium and UCYN-A) suggested that sub-populations are adapted to time- and depth-dependent environmental variation. A network analysis of the upper euphotic (0-75 m) HTS data identified two modules that reflect a diazotroph community structure with seasonal turnover between UCYN-A/Gamma A, andTrichodesmium/Crocosphaera . It also reveals the seasonality of several important cyanobacteria and NCDs about which little is known, including a putative δ-proteobacterial phylotype originally discovered at Stn. ALOHA. Collectively, these results underscore the importance of couplingnifH gene HTS with other molecular techniques to obtain a comprehensive view of diazotroph community composition in the marine environment and reveal several understudied diazotroph groups that may contribute to N2fixation in the NPSG. -
Abstract. Trichodesmium species, as a group of photosynthetic N2 fixers(diazotrophs), play an important role in the marine biogeochemical cycles ofnitrogen and carbon, especially in oligotrophic waters. How ongoing oceanwarming may interact with light availability to affect Trichodesmium is not yet clear. Wegrew Trichodesmium erythraeum IMS 101 at three temperature levels of 23, 27, and 31∘C undergrowth-limiting and growth-saturating light levels of 50 and 160 µmol quanta m−2 s−1, respectively, for at least 10 generations and thenmeasured physiological performance, including the specific growth rate, N2fixation rate, and photosynthesis. Light availability significantly modulatedthe growth response of Trichodesmium to temperature, with the specific growth ratepeaking at ∼27∘C under the light-saturatingconditions, while growth of light-limited cultures was non-responsive acrossthe tested temperatures (23, 27, and 31∘C). Short-term thermalresponses for N2 fixation indicated that both high growth temperatureand light intensity increased the optimum temperature (Topt) forN2 fixation and decreased its susceptibility to supra-optimaltemperatures (deactivation energy – Eh). Simultaneously, alllight-limited cultures with low Topt and high Eh were unable tosustain N2 fixation during short-term exposure to high temperatures (33–34∘C) that are not lethal for the cells grown underlight-saturating conditions. Our results imply that Trichodesmium spp. growing under lowlight levels while distributed deep in the euphotic zone or under cloudyweather conditions might be less sensitive to long-term temperature changesthat occur on the timescale of multiple generations but are more susceptible toabrupt (less than one generation time span) temperature changes, such asthose induced by cyclones and heat waves.more » « less
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ABSTRACT Trichodesmium is a globally distributed cyanobacterium whose nitrogen-fixing capability fuels primary production in warm oligotrophic oceans. Like many photoautotrophs, Trichodesmium serves as a host to various other microorganisms, yet little is known about how this associated community modulates fluxes of environmentally relevant chemical species into and out of the supraorganismal structure. Here, we utilized metatranscriptomics to examine gene expression activities of microbial communities associated with Trichodesmium erythraeum (strain IMS101) using laboratory-maintained enrichment cultures that have previously been shown to harbor microbial communities similar to those of natural populations. In enrichments maintained under two distinct CO 2 concentrations for ∼8 years, the community transcriptional profiles were found to be specific to the treatment, demonstrating a restructuring of overall gene expression had occurred. Some of this restructuring involved significant increases in community respiration-related transcripts under elevated CO 2 , potentially facilitating the corresponding measured increases in host nitrogen fixation rates. Particularly of note, in both treatments, community transcripts involved in the reduction of nitrate, nitrite, and nitrous oxide were detected, suggesting the associated organisms may play a role in colony-level nitrogen cycling. Lastly, a taxon-specific analysis revealed distinct ecological niches of consistently cooccurring major taxa that may enable, or even encourage, the stable cohabitation of a diverse community within Trichodesmium consortia. IMPORTANCE Trichodesmium is a genus of globally distributed, nitrogen-fixing marine cyanobacteria. As a source of new nitrogen in otherwise nitrogen-deficient systems, these organisms help fuel carbon fixation carried out by other more abundant photoautotrophs and thereby have significant roles in global nitrogen and carbon cycling. Members of the Trichodesmium genus tend to form large macroscopic colonies that appear to perpetually host an association of diverse interacting microbes distinct from the surrounding seawater, potentially making the entire assemblage a unique miniature ecosystem. Since its first successful cultivation in the early 1990s, there have been questions about the potential interdependencies between Trichodesmium and its associated microbial community and whether the host's seemingly enigmatic nitrogen fixation schema somehow involved or benefited from its epibionts. Here, we revisit these old questions with new technology and investigate gene expression activities of microbial communities living in association with Trichodesmium .more » « less
