DOCSLIB.ORG

Hopanoid Lipids May Facilitate Aerobic Nitrogen Fixation in the Ocean

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Hopanoid Lipids May Facilitate Aerobic Nitrogen Fixation in the Ocean Hopanoid lipids may facilitate aerobic nitrogen fixation BRIEF REPORT in the ocean Francisco M. Cornejo-Castilloa,1 and Jonathan P. Zehra,1 aDepartment of Ocean Sciences, University of California, Santa Cruz, CA 95064 Edited by Donald E. Canfield, Institute of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, Odense M., Denmark, and approved August 6, 2019 (received for review May 14, 2019) Cyanobacterial diazotrophs are considered to be the most impor- (12), but whether these mechanisms are sufficient to lower the O2 tant source of fixed N2 in the open ocean. Biological N2 fixation is concentration in the inner cell while N2 fixation takes place remains catalyzed by the extremely O2-sensitive nitrogenase enzyme. In unknown. cyanobacteria without specialized N2-fixing cells (heterocysts), mecha- We have discovered a consistent pattern of distribution of nisms such as decoupling photosynthesis from N2 fixationinspaceor hopanoid synthesis genes among marine cyanobacteria that sug- time are involved in protecting nitrogenase from the intracellular O2 gests that they may play an important role in marine N2 fixation. evolved by photosynthesis. However, it is not known how cyanobac- Hopanoids are a class of membrane lipids that have been shown to terial cells limit O2 diffusion across their membranes to protect nitroge- confer special properties to cell membranes (13). Hopanoids can nase in ambient O2-saturated surface ocean waters. Here, we explored intercalate into lipid bilayers of membranes due to their planar all known genomes of the major marine cyanobacterial lineages for the and hydrophobic structure and might decrease their permeability presence of hopanoid synthesis genes, since hopanoids are a class of to O2 (14). Approximately 10% of bacteria, including plant- lipids that might act as an O2 diffusion barrier. We found that, whereas associated diazotrophs, have the gene for the synthesis of hopanoids all non−heterocyst-forming cyanobacterial diazotrophs had hopanoid (the squalene−hopene cyclase gene shc) (13). Interestingly, the synthesis genes, none of the marine Synechococcus, Prochlorococcus only direct evidence showing that hopanoids facilitate N2 fixation (non−N -fixing), and marine heterocyst-forming (N -fixing) cyanobacteria 2 2 comes from studies of the terrestrial N2-fixing heterotrophic did. Finally, we conclude that hopanoid-enriched membranes are a bacteria Frankia.InFrankia sp., hopanoids might serve as an SCIENCES conserved trait in non−heterocyst-forming cyanobacterial diazotrophs ENVIRONMENTAL O2 diffusion barrier in their N2-fixing vesicles (15), with the that might lower the permeability to extracellular O2.Thismembrane thickness of the vesicle envelope directly correlated to the property coupled with high respiration rates to decrease intracellular external O concentration (16). However, this linkage was later − 2 O2 concentration may therefore explain how non heterocyst-forming questioned based on the observation of high proportions cyanobacterial diazotrophs can fix N2 in the fully oxic surface ocean. of hopanoids in membranes regardless of the N status in Frankia sp. (17). oxygen diffusion barrier | hopanoid lipids | nitrogen fixation | marine We compiled data on hopanoid production and mined the cyanobacteria publicly available genomes of marine cyanobacteria to provide an exploration of the presence of hopanoid biosynthetic and mod- arine cyanobacterial diazotrophs, i.e., those capable of ification genes across all of the major marine cyanobacterial line- Mreducing dissolved dinitrogen gas (N2) into ammonia ages, including both diazotrophs and non-diazotrophs (Fig. 1). We through N2 fixation, are key suppliers of bioavailable N, a lim- found that the shc gene for synthesizing hopanoids was consistently iting nutrient for primary production in the ocean (1). Biological present in all of the non−heterocyst-forming cyanobacterial diazo- N2 fixation is solely performed by the O2-sensitive nitrogenase en- trophs, including unicellular cyanobacterial symbionts with ex- zyme (2), and understanding how low intracellular O2 concentra- tremely reduced genomes such as UCYN-A. In contrast, none of tions are maintained in fully oxic open waters is a long-standing the non-diazotrophic marine Synechococcus and Prochlorococcus, question that has attracted much interest (3–6). which are the dominant cyanobacteria in the ocean (18, 19), nor the Although, a priori, it would seem that N2 fixation is incompatible heterocyst-forming marine cyanobacteria Calothrix rhizosoleniae with the O2-evolving photosynthetic lifestyle of cyanobacteria, it is SC01 and Richelia intracellularis HH01 had the shc gene in their known that these microorganisms have evolved a variety of strate- genomes. The same pattern was observed for almost all of the gies to protect nitrogenase from O2 inactivation. For example, some hopanoid modification genes except for the hpnK and hpnP genes filamentous cyanobacteria, including the symbionts of marine dia- (Fig. 1). These observations suggest that, whereas the capacity of toms, form specialized cells called heterocysts (7). A microaerobic allocating hopanoids into cell membranes may be universal across environment is created inside heterocysts by inactivating oxygenic all marine non−heterocyst-forming diazotrophic cyanobacteria, it is photosynthesis, by maintaining or enhancing respiration, and by the absent from all marine Synechococcus and Prochlorococcus (which formation of an extra glycolipid cell envelope outside the cell wall do not fix N2) and from heterocyst-forming marine cyanobacteria − (8). In contrast, non heterocyst-forming cyanobacteria such as the (which already protect nitrogenase from O2 by heterocysts). Fur- filamentous Trichodesmium or the free-living unicellular Croco- thermore, in Crocosphaera and Cyanothece, the transcription of the sphaera must separate photosynthesis and N2 fixation either spa- shc gene peaks right before the nitrogenase-encoding gene (nifH) tially or temporally to avoid exposing nitrogenase to the O2 that starts increasing its expression level (data collected from ref. 20), they produce during the light hours (9, 10). In the unicellular and simultaneous expression of both markers has also been cyanobacterial symbiont UCYN-A, all of the genes for the synthesis of the O2-evolving photosystem II (PSII) apparatus have been lost and so UCYN-A doesn’t generate O2 (11). None of the aforementioned Author contributions: F.M.C.-C. and J.P.Z. designed research, performed research, ana- strategies, however, can protect nitrogenase of non−heterocyst- lyzed data, and wrote the paper. forming cyanobacterial diazotrophs from the O2 that diffuses The authors declare no conflict of interest. across cell membranes from the environment (including host pho- This open access article is distributed under Creative Commons Attribution-NonCommercial- tosynthesis in the case of UCYN-A). Mechanisms such as respira- NoDerivatives License 4.0 (CC BY-NC-ND). 1 tion, the Mehler reaction, and/or other O2 scavenging strategies To whom correspondence may be addressed. Email: [email protected] or [email protected]. have been proposed as potential ways to overcome this problem www.pnas.org/cgi/doi/10.1073/pnas.1908165116 PNAS Latest Articles | 1of3 Downloaded by guest on September 25, 2021 Hopanoid biosynthesis SHC Squalene Diploptene or Diplopterol Hopanoid modification 2-Methyl-BHT 3-Methyl-BHT HpnP HpnR HpnH HpnG HpnO Diploptene Adenosylhopane Ribosylhopane Aminobacteriohopanetriol HpnI HpnK HpnJ BHT cyclitol N-acetylglucosaminyl BHT Glucosaminyl BHT ether Presence of hopanoid biosynthesis Hopanoid and modification genes production* Trichodesmium erythraeum IMS101 shc hpnH hpnG hpnP hpnI - hpnJ Yes Cyanothece sp. ATCC 51142 shc hpnH hpnG hpnP hpnI - hpnJ Yes Cyanothece sp. BG0011 shc hpnH hpnG hpnP hpnI - hpnJ n.t. Cyanothece sp. ATCC 51472 shc hpnH hpnG hpnP hpnI - hpnJ n.t. Cyanothece sp. CCY0110 shc hpnH hpnG hpnP hpnI - hpnJ n.t. Crocosphaera watsonii WH 8501 shc hpnH hpnG hpnP hpnI - hpnJ Yes Crocosphaera watsonii WH 0401 shc hpnH hpnG hpnP hpnI - hpnJ n.t. Crocosphaera watsonii WH 0003 shc hpnH hpnG hpnP hpnI - hpnJ n.t. UCYN-A1 shc hpnH hpnG - hpnI - hpnJ n.t. Diazotrophic cyanobacteriaDiazotrophic UCYN-A2 shc hpnH hpnG - hpnI - hpnJ n.t. Calothrix rhizosoleniae hpnP n.t. heterocyst- SC01 - - --- - forming Richelia intracellularis HH01 --- hpnP - - - n.t. Prochlorococcus marinus MED4 - - - - - - - No Prochlorococcus marinus AS9601 - - - - - - - n.t. Prochlorococcus sp. MIT 0801 - - - - - - - n.t. Prochlorococcus marinus MIT 9211 - - - - - - - n.t. Prochlorococcus marinus MIT 9313 - - - hpnP - hpnK - No Synechococcus sp. CC9605 - - - hpnP - hpnK - n.t. Synechococcus sp. WH 8102 - - - hpnP - hpnK - No Synechococcus sp. RS9917 - - - hpnP - hpnK - n.t. Non-diazotrophic cyanobacteria Synechococcus sp. RCC307 - - - hpnP - hpnK - n.t. Fig. 1. Hopanids in marine cyanobacteria. (Upper) A schematic representation of the hopanoid biosynthesis and modification pathways, including enzymes and products. (Lower) Summary of the presence/absence of the genes involved in the synthesis and modification of hopanoids across a selection of the major marine cyanobacterial lineages. All of the available marine cyanobacterial genomes in NCBI (May 2019) were screened for this analysis, yet only 21 are shown, for simplification. Asterisk (*), experimentally tested in refs. 20 and 21 (n.t., not tested). Enzymes participating in hopanoid pathways: squalene−hopene cyclase (SHC),
Load more

Recommended publications
  • Heterogeneous Nitrogen Fixation Rates Confer Energetic Advantage And
    ARTICLE https://doi.org/10.1038/s42003-020-0894-4 OPEN Heterogeneous nitrogen fixation rates confer energetic advantage and expanded ecological niche of unicellular diazotroph populations ✉ Takako Masuda1,2,5 , Keisuke Inomura3, Naoto Takahata 4, Takuhei Shiozaki1,4, Yuji Sano 4, 1234567890():,; Curtis Deutsch 3, Ondřej Prášil 2 & Ken Furuya1,6 Nitrogen fixing plankton provide nitrogen to fuel marine ecosystems and biogeochemical cycles but the factors that constrain their growth and habitat remain poorly understood. Here we investigate the importance of metabolic specialization in unicellular diazotroph popula- tions, using laboratory experiments and model simulations. In clonal cultures of Crocosphaera 15 15 watsonii and Cyanothece sp. spiked with N2, cellular N enrichment developed a bimodal distribution within colonies, indicating that N2 fixation was confined to a subpopulation. In a model of population metabolism, heterogeneous nitrogen (N2) fixation rates substantially reduce the respiration rate required to protect nitrogenase from O2. The energy savings from metabolic specialization is highest at slow growth rates, allowing populations to survive in deeper waters where light is low but nutrients are high. Our results suggest that hetero- geneous N2 fixation in colonies of unicellular diazotrophs confers an energetic advantage that expands the ecological niche and may have facilitated the evolution of multicellular diazotrophs. 1 Department of Aquatic Bioscience, The University of Tokyo, Yayoi, Bunkyo, Tokyo 113-8657, Japan. 2 Institute of Microbiology, The Czech Academy of Sciences, Opatovický mlýn, 379 01 Třeboň, Czech Republic. 3 School of Oceanography, University of Washington, Seattle, WA, USA. 4 Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwanoha, Kashiwa-shi, Chiba 277-8564, Japan.
    [Show full text]
  • University of California Santa Cruz
    UNIVERSITY OF CALIFORNIA SANTA CRUZ MOLECULAR BIOMARKERS FOR PHOSPHORUS STRESS IN THE MARINE CYANOBACTERIUM CROCOSPHAERA A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in OCEAN SCIENCES by Nicole A. Pereira December 2017 The dissertation of Nicole A. Pereira is approved: Professor Jonathan P. Zehr, Chair Professor Raphael M. Kudela Professor Chad Saltikov Tyrus Miller Vice Provost and Dean of Graduate Studies Copyright © by Nicole A. Pereira 2017 TABLE OF CONTENTS List of Tables and Figures ...................................................................................... vi Abstract ................................................................................................................ viii Acknowledgements ................................................................................................ ix INTRODUCTION .............................................................................................. 1 References ............................................................................................................ 6 CHAPTER 1: MOLECULAR MARKERS DEFINE PROGRESSING STAGES OF PHOSPHORUS LIMITATION IN THE NITROGEN- FIXING CYANOBACTERIUM, CROCOSPHAERA WATSONII .............. 11 Abstract .............................................................................................................. 12 1. Introduction .................................................................................................. 12 2. Materials and Methods ................................................................................
    [Show full text]
  • (Cyanobacterial Genera) 2014, Using a Polyphasic Approach
    Preslia 86: 295–335, 2014 295 Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach Taxonomické hodnocení cyanoprokaryot (cyanobakteriální rody) v roce 2014 podle polyfázického přístupu Jiří K o m á r e k1,2,JanKaštovský2, Jan M a r e š1,2 & Jeffrey R. J o h a n s e n2,3 1Institute of Botany, Academy of Sciences of the Czech Republic, Dukelská 135, CZ-37982 Třeboň, Czech Republic, e-mail: [email protected]; 2Department of Botany, Faculty of Science, University of South Bohemia, Branišovská 31, CZ-370 05 České Budějovice, Czech Republic; 3Department of Biology, John Carroll University, University Heights, Cleveland, OH 44118, USA Komárek J., Kaštovský J., Mareš J. & Johansen J. R. (2014): Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. – Preslia 86: 295–335. The whole classification of cyanobacteria (species, genera, families, orders) has undergone exten- sive restructuring and revision in recent years with the advent of phylogenetic analyses based on molecular sequence data. Several recent revisionary and monographic works initiated a revision and it is anticipated there will be further changes in the future. However, with the completion of the monographic series on the Cyanobacteria in Süsswasserflora von Mitteleuropa, and the recent flurry of taxonomic papers describing new genera, it seems expedient that a summary of the modern taxonomic system for cyanobacteria should be published. In this review, we present the status of all currently used families of cyanobacteria, review the results of molecular taxonomic studies, descriptions and characteristics of new orders and new families and the elevation of a few subfamilies to family level.
    [Show full text]
  • UC Santa Cruz UC Santa Cruz Electronic Theses and Dissertations
    UC Santa Cruz UC Santa Cruz Electronic Theses and Dissertations Title Comparative genomics and natural distributions of phenotypically distinct strains of the nitrogen-fixing cyanobacterium Crocosphaera watsonii Permalink https://escholarship.org/uc/item/2sh8r9q6 Author Bench, Shellie Publication Date 2012 Supplemental Material https://escholarship.org/uc/item/2sh8r9q6#supplemental Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA SANTA CRUZ COMPARATIVE GENOMICS AND NATURAL DISTRIBUTIONS OF PHENOTYPICALLY DISTINCT STRAINS OF THE NITROGEN-FIXING CYANOBACTERIUM CROCOSPHAERA WATSONII A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in OCEAN SCIENCES by Shellie R. Bench June 2012 The Dissertation of Shellie R. Bench is approved: ______________________________ Professor Jonathan P. Zehr, Chair ______________________________ Professor Fitnat Yildiz ______________________________ Professor Jack Meeks ______________________________ Professor Eric Webb ______________________________ Tyrus Miller Vice Provost and Dean of Graduate Studies Copyright © by Shellie R. Bench 2012 Table of Contents Title ........................................................................................................................ i Copyright .............................................................................................................. ii Table of contents .................................................................................................
    [Show full text]
  • Low Genomic Diversity in Tropical Oceanic N2-Fixing Cyanobacteria Jonathan P
    Low genomic diversity in tropical oceanic N2-fixing cyanobacteria Jonathan P. Zehr*†, Shellie R. Bench*, Elizabeth A. Mondragon*, Jay McCarren‡, and Edward F. DeLong‡ *Department of Ocean Sciences, University of California, 1156 High Street, Santa Cruz, CA 95064; and ‡Department of Civil and Environmental Engineering and Division of Biological Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved September 7, 2007 (received for review April 9, 2007) High levels of genomic and allelic microvariation have been Given the large degree of sequence and genome divergence found in major marine planktonic microbial species, including that coincides with ecotypes in Prochlorococcus (3), we hypoth- the ubiquitous open ocean cyanobacterium, Prochlorococcus esized that there would be similar genetic diversity and ecotypic marinus. Crocosphaera watsonii is a unicellular cyanobacterium variability within the unicellular diazotrophic cyanobacterial that has recently been shown to be important in oceanic N2 genus Crocosphaera. However, by comparing amplified gene fixation and has been reported from the Atlantic and Pacific sequences from cultivated strains and complete sequences of two oceans in both hemispheres, and the Arabian Sea. In direct metagenomic fragments, we found that the genomic sequence contrast to the current observations of genomic variability in diversity within this group of microorganisms appears to be marine non-N2-fixing planktonic cyanobacteria, which can range extremely low relative to the more abundant sympatric non-N2- up to >15% nucleotide sequence divergence, we discovered fixing cyanobacteria. that the marine planktonic nitrogen-fixing cyanobacterial genus Results and Discussion Crocosphaera has remarkably low genomic diversity, with <1% nucleotide sequence divergence in several genes among widely C.
    [Show full text]
  • Measuring Carbon and N2 Fixation in Field Populations of Colonial and Free-Living Unicellular Cyanobacteria Using Nanometer-Scale Secondary Ion Mass Spectrometry1
    J. Phycol. 49, 502–516 (2013) © 2013 Phycological Society of America DOI: 10.1111/jpy.12057 MEASURING CARBON AND N2 FIXATION IN FIELD POPULATIONS OF COLONIAL AND FREE-LIVING UNICELLULAR CYANOBACTERIA USING NANOMETER-SCALE SECONDARY ION MASS SPECTROMETRY1 Rachel A. Foster,2 Saar Sztejrenszus,3 and Marcel M. M. Kuypers Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Celsiusstr 1, Bremen D-28359, Germany Unicellular cyanobacteria are now recognized as ocean, cyanobacteria are one of the dominant important to the marine N and C cycles in open N2-fixing (diazotroph) groups of organisms where ocean gyres, yet there are few direct in situ abundances of several lineages, including filamen- measurements of their activities. Using a high-resolution tous and unicellular types, often co-occur. The nanometer scale secondary ion mass spectrometer larger filamentous and symbiotic types (i.e., Trich- (nanoSIMS), single cell N2 and C fixation rates were odesmium spp. and Richelia intracellularis) have long estimated for unicellular cyanobacteria resembling been considered the primary N2 fixers in open Crocosphaera watsonii Crocosphaera watsonii N2 fixer . - ocean gyres (Mague et al. 1974, Capone et al. 1997, like cells were observed in the subtropical North Karl et al. 2002). However, more recently, unicellu- Pacific gyre (22°45′ N, 158°0′ W) as 2 different lar cyanobacteria are now thought of as an equally phenotypes: colonial and free-living. Colonies important new source of N due to their high abun- containing 3–242 cells per colony were observed and dances and broad distributions (Needoba et al. cell density in colonies increased with incubation 2007, Moisander et al.
    [Show full text]
  • Daily Cycle of Carbon and Nitrogen Fixation in the Unicellular Cyanobacterium: Crocosphaera Watsonii Wh8501
    UvA-DARE (Digital Academic Repository) Oxygen and temperature in relation to nitrogen fixation in cyanobacteria: In the daily life of cyanobacteria Compaoré, J. Publication date 2010 Link to publication Citation for published version (APA): Compaoré, J. (2010). Oxygen and temperature in relation to nitrogen fixation in cyanobacteria: In the daily life of cyanobacteria. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:30 Sep 2021 Chapter 4 DAILY CYCLE OF CARBON AND NITROGEN FIXATION IN THE UNICELLULAR CYANOBACTERIUM: CROCOSPHAERA WATSONII WH8501 1 1 1 1 Justine Compaoré , Henricus T. S. Boschker , Anita Wijnholds , Tanja Moerdijk-Poortvliet and Lucas J. Stal 1, 2* 1Netherlands Institute for Ecology, NIOO-KNAW, Department of Marine Microbiology, P.O. Box 140, 4400 AC Yerseke, The Netherlands 2Department of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands To be submitted Running Title : Daily cycle of carbon and nitrogen fixation in Crocosphaera sp.
    [Show full text]
  • 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).
    [Show full text]
  • 1 Supplementary Material
    Supplementary material: Supplementary Methods Derivation of the key equation Here we describe the derivation of Equation (1) in the main text. Figure S1 shows a schematic of CFM- 푗 -1 푗푘 -1 - DDA with flux notations. Below 푄푖 (pmol cell ) indicates the cellular quota of i in j, and 퐽푖 (pmol cell d 1) indicates transport of i from j to k, where i = C or N and j,k = H (Heterocysts: Het), V (Vegetative cells: Veg) or D (Diatoms: Dia). We start with describing time dependences of each element in each cell. The 퐻 푁2푓푖푥 -1 -1 balance of 푄퐶 is based on C transfer and cost of N2 fixation 퐹퐶 (pmol N cell d ), which includes C cost for providing electron and energy through respiration: 퐻 푑푄퐶 = 퐽푉퐻 − 퐹푁2푓푖푥 [Eq. S1] 푑푡 퐶 퐶 퐻 Similarly, the time dependence of 푄푁 is based on the balance between fixed N transport and N2 fixation 푁2푓푖푥 -1 -1 퐹푁 (pmol N cell d ): 퐻 푑푄푁 = −퐽퐻푉 + 퐹푁2푓푖푥 [Eq. S2] 푑푡 푁 푁 Veg needs to produce biomass both for new Veg and Het. Also, they can fix C. Thus, the time variation of C in Veg is as follows: 푉 푑푄퐶 = 퐹푉 + 퐽퐷푉 − 퐽푉퐻 − 휇(푄푉 + 푄퐻)(1 + 퐸) [Eq. S3] 푑푡 푃ℎ표 퐶 퐶 퐶 퐶 푉 -1 -1 -1 where 퐹푃ℎ표 (pmol C cell d ) is photosynthesis (C fixation) by Veg, μ (d ) is growth rate and E (dimensionless) is respiration factor. This equation also includes the transfer of C from Dia and transfer of C to Het.
    [Show full text]
  • Differing Responses of Marine N2 Fixers to Warming and Consequences for Future Diazotroph Community Structure
    Vol. 72: 33–46, 2014 AQUATIC MICROBIAL ECOLOGY Published online March 7 doi: 10.3354/ame01683 Aquat Microb Ecol Differing responses of marine N2 fixers to warming and consequences for future diazotroph community structure Fei-Xue Fu*, Elizabeth Yu, Nathan S. Garcia, Jasmine Gale, Yunsheng Luo, Eric A. Webb, David A. Hutchins Department of Biological Sciences, The University of Southern California, 3616 Trousdale Parkway, Los Angeles, California 90089, USA ABSTRACT: The globally distributed colonial cyanobacterium Trichodesmium and unicellular diazotrophs including Crocosphaera together carry out the majority of marine biological nitrogen (N2) fixation. Future sea surface warming is predicted to influence their abundance and distribu- tion, but temperature reaction norms have been determined for very few representatives of each genus. We compared thermal responses within and between the 2 genera Trichodesmium and Crocosphaera by measuring reaction norms for growth, N2 fixation, carbon fixation, and elemental ratios in 7 strains from a global culture collection. Temperature reaction norms of Trichodesmium and Crocosphaera were remarkably similar for all isolates within each genus, regardless of their geographic origin. Thermal limits of Trichodesmium and Crocosphaera ranged from 18 to 32°C and 24 to 32°C, and optimum growth temperatures were ~26 and ~30°C, respectively. The highest cellular ratios of nitrogen to phosphorus and carbon to nitrogen were found at optimum growth temperatures, and the lowest ratios near their thermal limits. In a mixed competition experiment, Trichodesmium growth rates were ~25% higher than those of Crocosphaera at 24°C, while those of Crocosphaera were ~50% higher at 28°C. Comparison of these results to current and projected seasonal temperature regimes in the subtropical Atlantic and Pacific Oceans suggests that pre- dicted warmer temperatures may favor Crocosphaera over Trichodesmium, but that both genera may be excluded where future temperatures consistently exceed 32°C.
    [Show full text]
  • Hydrogen Production by Trichodesmium Erythraeum Cyanothece Sp
    Vol. 59: 197–206, 2010 AQUATIC MICROBIAL ECOLOGY Published online April 8 doi: 10.3354/ame01407 Aquat Microb Ecol Hydrogen production by Trichodesmium erythraeum Cyanothece sp. and Crocosphaera watsonii Samuel T. Wilson1, 2,*, Rachel A. Foster1, 3, Jonathan P. Zehr1, 3, David M. Karl1, 2 1Center for Microbial Oceanography: Research and Education, Honolulu, Hawaii 96822, USA 2Department of Oceanography, 1000 Pope Road, University of Hawaii, Honolulu, Hawaii 96822, USA 3Ocean Sciences, University of California, Santa Cruz, California 95064, USA ABSTRACT: Diazotrophic cyanobacteria are important components of marine ecosystems, where they contribute to primary production and provide a source of fixed nitrogen (N). During biological fixation of atmospheric nitrogen (N2), hydrogen is produced as an obligate by-product. The present study investigated the potential contribution of 4 marine diazotrophs to the pool of dissolved H2 in the oceans. N2 fixation, as measured by acetylene reduction, and H2 production rates were monitored throughout the diel period in cultures of the filamentous Trichodesmium erythraeum strain IMS101, and the unicellular organisms Cyanothece sp. strain ATCC 51142 and Crocosphaera watsonii strains WH8501 and WH0002. H2 production coincided with diel variations in N2 fixation for each strain regardless of whether N2 fixation peaked during the day or night. Chlorophyll-normalized rates of H2 production ranged 100-fold from a maximum of 3 nmol µg chl a–1 h–1 in T. erythraeum IMS101 cul- –1 –1 tures to 0.03 nmol µg chl a h in Crocosphaera watsonii WH0002. Overall, the ratio of net H2 pro- duced to N2 fixed varied from 0.05 to 0.003 in the unicellular cyanobacteria, compared to 0.3 in the filamentous T.
    [Show full text]
  • Physiological Response of Crocosphaera Watsonii to Enhanced and Fluctuating Carbon Dioxide Conditions
    Physiological Response of Crocosphaera watsonii to Enhanced and Fluctuating Carbon Dioxide Conditions Gradoville, M. R., White, A. E., Letelier, R. M. (2014). Physiological Response of Crocosphaera watsonii to Enhanced and Fluctuating Carbon Dioxide Conditions. PLoS ONE, 9(10), e110660. doi:10.1371/journal.pone.0110660 10.1371/journal.pone.0110660 Public Library of Science Version of Record http://cdss.library.oregonstate.edu/sa-termsofuse Physiological Response of Crocosphaera watsonii to Enhanced and Fluctuating Carbon Dioxide Conditions Mary R. Gradoville*, Angelicque E. White, Ricardo M. Letelier Oregon State University, College of Earth, Ocean, and Atmospheric Sciences, Corvallis, Oregon, United States of America Abstract We investigated the effects of elevated pCO2 on cultures of the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH8501. Using CO2-enriched air, cultures grown in batch mode under high light intensity were exposed to initial conditions approximating current atmospheric CO2 concentrations (,400 ppm) as well as CO2 levels corresponding to low- and high- end predictions for the year 2100 (,750 and 1000 ppm). Following acclimation to CO2 levels, the concentrations of particulate carbon (PC), particulate nitrogen (PN), and cells were measured over the diurnal cycle for a six-day period spanning exponential and early stationary growth phases. High rates of photosynthesis and respiration resulted in biologically induced pCO2 fluctuations in all treatments. Despite this observed pCO2 variability, and consistent with previous experiments conducted under stable pCO2 conditions, we observed that elevated mean pCO2 enhanced rates of PC production, PN production, and growth. During exponential growth phase, rates of PC and PN production increased by ,1.2- and ,1.5-fold in the mid- and high-CO2 treatments, respectively, when compared to the low-CO2 treatment.
    [Show full text]