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Crocosphaera Watsonii Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii Mak A. Saitoa,1, Erin M. Bertranda, Stephanie Dutkiewiczb, Vladimir V. Bulygina,2, Dawn M. Morana, Fanny M. Monteirob, Michael J. Followsb, Frederica W. Valoisc, and John B. Waterburyc aMarine Chemistry and Geochemistry Department and cBiology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; and bEarth Atmospheric and Planetary Sciences Department, Massachusetts Institute of Technology (MIT), 77 Massachusetts Avenue, Cambridge, MA 02139 Edited* by Paul G. Falkowski, Rutgers, State University of New Jersey, Brunswick, NJ, and approved November 19, 2010 (received for review May 31, 2010) The marine nitrogen fixing microorganisms (diazotrophs) are a sistent with theoretical studies predicting a large iron require- major source of nitrogen to open ocean ecosystems and are pre- ment in marine diazotrophs (13, 18), it has been somewhat dicted to be limited by iron in most marine environments. Here controversial due to the implication of a dynamic yet poorly un- we use global and targeted proteomic analyses on a key unicellular derstood diel cycle for intracellular iron. Several unicellular dia- marine diazotroph Crocosphaera watsonii to reveal large scale diel zotrophs, including Crocosphaera watsonii, have been observed to changes in its proteome, including substantial variations in concen- fix nitrogen during the dark period (Fig. 1A), and this is widely trations of iron metalloproteins involved in nitrogen fixation and viewed as an adaption for temporal separation of photosynthesis photosynthesis, as well as nocturnal flavodoxin production. The and nitrogen fixation to avoid the oxygen disruption of the nitro- daily synthesis and degradation of enzymes in coordination with genase complex (6, 19, 20). Global transcriptional studies have their utilization results in a lowered cellular metalloenzyme inven- also observed large scale changes in the transcriptomes of the uni- tory that requires ∼40% less iron than if these enzymes were main- cellular diazotrophs Crocosphaera watsonii (21), Cyanothece (22), tained throughout the diel cycle. This strategy is energetically Gloeothece (23), and a hot-spring Synechococcus (24) during the expensive, but appears to serve as an important adaptation for confronting the iron scarcity of the open oceans. A global numer- diel cycle, consistent with a temporal separation of photosynth- ical model of ocean circulation, biogeochemistry and ecosystems esis and nitrogen fixation. Yet the possibility that diel cycling of suggests that Crocosphaera’s ability to reduce its iron-metalloen- the transcriptome or proteome might affect the iron requirement zyme inventory provides two advantages: It allows Crocosphaera has not been previously discussed, likely because transcriptional to inhabit regions lower in iron and allows the same iron supply to studies provide information about gene expression rather than support higher Crocosphaera biomass and nitrogen fixation than actual enzyme inventories, and immunological protein studies if they did not have this reduced iron requirement. thus far, while having detected diel oscillations of the NifH subunit in Crocosphaera and Gloeothece (23, 25), are limited cyanobacteria ∣ marine iron cycle ∣ nitrogen cycle to a few select proteins with no global or absolute quantitative proteome studies of diazotrophs published as of yet. As a result, he biological fixation of atmospheric dinitrogen into ammonia it has remained uncertain whether the observed diel transcrip- Thas a major impact on the extent of marine primary produc- tome cycling was needed for the maintenance of a relatively con- tion (1, 2). Only a small number of bacteria are known to sistent proteome or was in fact causing large changes in the global contribute to nitrogen fixation in open ocean environments, proteome composition during each diel cycle. and they typically comprise a tiny fraction (<0.1%) of the overall Recent advances in proteomic technologies hold promise for microbial community (3, 4). Among these, the unicellular diazo- elucidating mechanistic connections between the biochemistry of troph Crocosphaera watsonii is estimated to be a significant important microbes and global biogeochemical cycles. There are contributor to oceanic nitrogen fixation (4–6). Whereas much two broad approaches to mass spectrometry based proteomics: of the primary productivity in the tropical and subtropical regions global shotgun proteomic approaches that can semiquantitatively ’ of the oceans is predicted to be nitrogen limited, the diazotrophs survey the relative abundance of hundreds of proteins simulta- nitrogen source, resupplied from the large atmospheric reservoir, neously using spectral counting (26), and targeted approaches is essentially limitless. Instead, iron is considered the critical that use selected reaction monitoring (SRM) mass spectrometry micronutrient for marine diazotrophs due to their use of the iron- with isotopically labeled peptide standards for absolute quantifi- nitrogenase protein complex containing a homodimeric iron pro- cation of proteins of interest (27). Though there are several tein with a 4Fe∶4S metallocluster (NifH) and a heterotetrameric molybdenum-iron protein with an 8Fe∶7S P cluster and a 7 Fe culture-based studies of marine microbes (26, 28) and field as- and 1 Mo MoFe cofactor (NifDK, α and β subunits) (7, 8) sessments of abundant proteins (29, 30), the combined applica- (Table S1). Field experiments and models both predict the distri- tion of global and targeted proteomic approaches to problems of bution of oceanic nitrogen fixation to be primarily constrained by – the availability of iron (2, 9 11). Despite this importance of iron Author contributions: M.A.S., E.M.B., S.D., and J.B.W. designed research; M.A.S., E.M.B., on marine nitrogen fixation, there is a limited understanding of S.D., V.V.B., D.M.M., F.M.M., M.J.F., F.W.V., and J.B.W. performed research; M.A.S., how marine diazotrophs have adapted to this low iron environ- E.M.B., S.D., V.V.B., and D.M.M. analyzed data; and M.A.S., E.M.B., and S.D. wrote ment (12–17). the paper. The coexistence of oxygenic photosynthesis and nitrogen The authors declare no conflict of interest. fixation metabolisms presents a unique challenge for diazotrophs *This Direct Submission article had a prearranged editor. due to their high iron demands and the chemical incompatibility Freely available online through the PNAS open access option. of molecular oxygen and the nitrogenase protein complex. Pre- 1To whom correspondence should be addressed. E-mail: [email protected]. vious elemental studies measuring whole cell iron content in 2Deceased June 28, 2009. Crocosphaera found increased iron during the dark period when This article contains supporting information online at www.pnas.org/lookup/suppl/ nitrogen fixation is occurring (15). Whereas this finding was con- doi:10.1073/pnas.1006943108/-/DCSupplemental. 2184–2189 ∣ PNAS ∣ February 8, 2011 ∣ vol. 108 ∣ no. 6 www.pnas.org/cgi/doi/10.1073/pnas.1006943108 Downloaded by guest on September 27, 2021 ) A -1 2000 hr -1 ) -1 1500 1000 mol ethylene cell mol ethylene -13 500 Glycogen (fgGlycogen cell 0 Fixation (10 Fixation 2 N 0 5 10 15 20 25 Hours B 100 80 60 40 Dark Period 20 Relative Protein Abundance Abundance Protein Relative 0 0 20406080100120 Relative Protein Abundance Light Period Fig. 1. Variations in the Crocosphaera proteome between the light and dark photoperiod. (A) Dark period nitrogen fixation (black) and glycogen storage (red) during a diel cycle (dark, black bar). (B) Relative protein abundance dur- ing light and dark periods, where similar expression (solid line, black circles; SCIENCES also see Fig. S1A for comparison of technical replicates) is contrasted by a ENVIRONMENTAL number of proteins (colors), including the nitrogenase complex metalloen- zymes (blue) and flavodoxin (yellow), with greater than 2-fold change in re- lative abundance (dashed lines) above a threshold of 5 normalized spectral counts in at least one treatment. Data are mean of six technical replicates. Fig. 2. Cluster analysis of global proteome during the diel cycle. Color marine biogeochemical relevance, such as the iron limitation of indicates higher (yellow) or lower (blue) relative abundance relative to marine diazotrophy, has not yet been reported. the centered mean value (black). Horizontal axis is hours from onset of light (L) or dark (D) period. Proteome data was filtered for proteins with at least Results and Discussion three time points having greater than 10 spectral counts and a difference The diel cycle and inventory of iron metalloenzymes in Croco- between maximum and minimum signals ≥14 spectral counts, prior to log sphaera watsonii were investigated using global and targeted transformation and normalization. Two major clusters were observed corre- liquid chromatography mass spectrometry (LC-MS) proteomic sponding to the light and dark photoperiods. techniques from three distinct culture experiments all grown ≥10 on a 14∶10 light∶dark cycle: a day-night experiment sampled dur- spectral count signal ( ) and displayed a diel variation in ≥ 14 ing the light and dark photoperiod (sampled 10 h from lights on amplitude (max - min ). Cluster analysis revealed two major and 7 h from lights off) analyzed for global proteome using both groups that include key photosystem or nitrogen fixation proteins 1D and 2D LC-MS approaches, a time course study (diel hereon) with
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