Fossilized glycolipids reveal past oceanic N2 fixation by heterocystous cyanobacteria
Edited by John M. Hayes, Woods Hole Oceanographic Institution, Berkeley, CA, and approved September 7, 2010 (received for review May 31, 2010)
Abstract
N2-fixing cyanobacteria play an essential role in sustaining primary productivity in contemporary oceans and freshwater systems. However, the significance of N2-fixing cyanobacteria in past nitrogen cycling is difficult to establish as their preservation potential is relatively poor and specific biological markers are presently lacking. Heterocystous N2-fixing cyanobacteria synthesize unique long-chain glycolipids in the cell envelope covering the heterocyst cell to protect the oxygen-sensitive nitrogenase enzyme. We found that these heterocyst glycolipids are remarkably well preserved in (ancient) lacustrine and marine sediments, unambiguously indicating the (past) presence of N2-fixing heterocystous cyanobacteria. Analysis of Pleistocene sediments of the eastern Mediterranean Sea showed that heterocystous cyanobacteria, likely as epiphytes in symbiosis with planktonic diatoms, were particularly abundant during deposition of sapropels. Eocene Arctic Ocean sediments deposited at a time of large Azolla blooms contained glycolipids typical for heterocystous cyanobacteria presently living in symbiosis with the freshwater fern Azolla, indicating that this symbiosis already existed in that time. Our study thus suggests that heterocystous cyanobacteria played a major role in adding “new” fixed nitrogen to surface waters in past stratified oceans.
Acknowledgments.
We thank three anonymous reviewers and the Editor for comments which improved this manuscript. H. Vogel, B. Wagner, M. Melles, P. De Deckker, C. Slomp, H. Mort, J. Werne, Y. van Breugel, J. Weijers, D. Verschuren, G. de Lange, and L. Schwark are acknowledged for supplying a number of the studied sediments; L. Stal and J. Campaore for providing cyanobacterial cultures, and M. van Kempen for providing cultured Azolla. Sediments were recovered from Lake Challa as part of the CHALLACEA project. Sediments from the Eocene Arctic were provided by the Integrated Ocean Drilling Program (IODP). Financial support for this research was provided by the Darwin Center for Biogeosciences, the Royal NIOZ, and the University of Utrecht awarded (to J.S.S.D. and G.J.R.). G.J.R. acknowledges the Statoil Company for additional financial support.
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References
1
C Deutsch, JL Sarmiento, DM Sigman, N Gruber, JP Dunne, Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007).
2
DG Capone, et al., Nitrogen fixation by Trichodesmium spp: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochem Cy 19, GB2024, doi:. (2005).
3
MJ Church, KM Bjorkman, DM Karl, MA Saito, JP Zehr, Regional distributions of nitrogen-fixing bacteria in the Pacific Ocean. Limnol Oceanogr 53, 63–77 (2008).
4
H Ploug, Cyanobacterial surface blooms formed by Aphanizomenon sp and Nodularia spumigena in the Baltic Sea: small-scale fluxes, pH, and oxygen microenvironments. Limnol Oceanogr 53, 914–921 (2008).
5
TA Villareal Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs, eds EJ Carpenter, DG Capone, JG Rueter (Kluwer Academic, Dordrecht, The Netherlands), pp. 163–175 (1992).
6
A Tomitani, AH Knoll, CM Cavanaugh, T Ohno, The evolutionary diversification of cyanobacteria: molecular phylogenetic and paleontological perspectives. Proc Nat Acad Sci USA 103, 5442–5447 (2006).
7
JP Sachs, DJ Repeta, Oligotrophy and nitrogen fixation during eastern Mediterranean sapropel events. Science 286, 2485–2488 (1999).
8
MMM Kuypers, Y van Breugel, S Schouten, E Erba, JS Sinninghe Damsté, N2-fixing cyanobacteria supplied nutrient N for Cretaceous oceanic anoxic events. Geology 32, 853–856 (2004).
9
GH Rau, MA Arthur, WA Dean, 15N/14N variations in Cretaceous Atlantic sedimentary sequences: implications for past changes in marine nitrogen biogeochemistry. Earth Planet Sc Lett 82, 269–279 (1987).
10
E Wada, A Hattori, Natural abundance of 15N in particulate organic matter in the North Pacific Ocean. Geochim Cosmochim Acta 40, 249–251 (1976).
11
RE Summons, LL Jahnke, JM Hope, GA Logan, 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400, 554–557 (1999).
12
AE Walsby, Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends Microbiol 15, 340–349 (2007).
13
A Gambacorta, E Pagnotta, I Romano, A Trincone, Heterocyst glycolipids from nitrogen-fixing cyanobacteria other than Nostocaceae. Phytochemistry 48, 801–805 (1998).
14
T Bauersachs, et al., Rapid analysis of long-chain glycolipids in heterocystous cyanobacteria using high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 23, 1387–1394 (2009).
15
T Bauersachs, S Schouten, J Compaoré, LJ Stal, JS Sinninghe Damsté, Distribution of heterocyst glycolipids in cyanobacteria. Phytochemistry 70, 1370–1376 (2009).
16
L Hoffmann, Marine cyanobacteria in tropical regions: diversity and ecology. Eur J Phycol 34, 371–379 (1999).
17
C Arnosti, BB Jørgensen, Organic carbon degradation in arctic marine sediments, Svalbard: A comparison of initial and terminal steps. Geomicrobiol J 23, 551–563 (2006).
18
HR Harvey, RD Fallon, JS Patton, The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments. Geochim Cosmochim Acta 50, 795–804 (1986).
19
S Schouten, J Middelburg, EC Hopmans, JS Sinninghe Damsté, Fossilization and degradation of intact polar lipids in deep subsurface sediments: a theoretical approach. Geochim Cosmochim Acta 74, 3806–3814 (2010).
20
JS Lipp, Y Morono, F Inagaki, K-U Hinrichs, Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature 454, 991–994 (2008).
21
A Pearson, Biogeochemistry—Who lives in the sea floor? Nature 454, 952–953 (2008).
22
M Rossignol-Strick, W Nesteroff, P Olive, C Vergnaudgrazzini, After the deluge—Mediterranean stagnation and sapropel formation. Nature 295, 105–110 (1982).
23
RC Thunell, DF Williams, PR Belyea, Anoxic events in the Mediterranean Sea in relation to the evolution of Late Neogene climates. Mar Geol 59, 105–134 (1984).
24
EJ Carpenter, S Janson, Anabaena gerdii sp nov., a new planktonic filamentous cyanobacterium from the South Pacific Ocean and Arabian Sea. Phycologia 40, 105–110 (2001).
25
MTJ van der Meer, et al., Hydrogen isotopic compositions of long-chain alkenones record freshwater flooding of the Eastern Mediterranean at the onset of sapropel deposition. Earth Planet Sc Lett 262, 594–600 (2007).
26
AES Kemp, RB Pearce, I Koizumi, J Pike, SJ Rance, The role of mat-forming diatoms in the formation of Mediterranean sapropels. Nature 398, 57–61 (1999).
27
H Brinkhuis, et al., Episodic fresh surface waters in the Eocene Arctic Ocean. Nature 441, 606–609 (2006).
28
EN Speelman, GJ Reichart, JW de Leeuw, WIC Rijpstra, JS Sinninghe Damsté, Biomarker lipids of the freshwater fern Azolla and its fossil counterpart from the Eocene Arctic Ocean. Org Geochem 40, 628–637 (2009).
29
EN Speelman, et al., The Eocene Arctic Azolla bloom: environmental conditions, productivity and carbon drawdown. Geobiology 7, 155–170 (2009).
30
CE Stickley, N Koc, HJ Brumsack, RW Jordan, I Suto, A siliceous microfossil view of middle Eocene Arctic paleoenvironments: a window of biosilica production and preservation. Paleoceanography 23, PA1S14, doi:https://doi.org/10.1029/2007PA001485. (2008).
31
J Knies, U Mann, BN Popp, R Stein, H-J Brumsack, Surface water productivity and paleoceanographic implications in the Cenozoic Arctic Ocean. Paleoceanography 23, PA1S16, doi:https://doi.org/10.1029/2007PA001455. (2008).
32
EB Braun-Howland, SA Nierzwicki-Bauer, Azolla-Anabaena azaollae symbiosis: biochemistry, ultrastructure, and molecular biology. Handbook of symbiotic cyanobacteria, ed AN Rai (CRC Press, Boca Raton, FL), pp. 65–118 (1990).
33
GA Peters, JC Meeks, Azolla-Anabaena symbiosis: basic biology. Annu Rev Plant Physiol Plant Mol Biol 40, 193–210 (1989).
34
GM Wagner, Azolla: a review of its biology and utilization. Bot Rev 63, 1–26 (1997).
35
R Rippka, J Deruelles, JB Waterbury, M Herdman, RY Stanier, Generic assignments, strain histories, and properties of pure cultures of cyanobacteria. J Gen Microbiol 111, 1–61 (1979).
36
J Backman, K Moran, DB McInroy, LA Mayer, Arctic coring expedition. Proc Integr Ocean Drill Progr 302, (doi:, Integrated Ocean Drilling Program Management International Inc., Edinburgh). (2006).
37
EG Bligh, WJ Dyer, A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37, 911–917 (1959).
38
H Rütters, H Sass, H Cypionka, J Rullkötter, Phospholipid analysis as a tool to study complex microbial communities in marine sediments. J Microbiol Meth 48, 149–160 (2002).
39
HF Sturt, RE Summons, K Smith, M Elvert, KU Hinrichs, Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry—new biomarkers for biogeochemistry and microbial ecology. Rapid Commun Mass Spectrom 18, 617–628 (2004).
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Published online: October 21, 2010
Published in issue: November 9, 2010
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Acknowledgments
We thank three anonymous reviewers and the Editor for comments which improved this manuscript. H. Vogel, B. Wagner, M. Melles, P. De Deckker, C. Slomp, H. Mort, J. Werne, Y. van Breugel, J. Weijers, D. Verschuren, G. de Lange, and L. Schwark are acknowledged for supplying a number of the studied sediments; L. Stal and J. Campaore for providing cyanobacterial cultures, and M. van Kempen for providing cultured Azolla. Sediments were recovered from Lake Challa as part of the CHALLACEA project. Sediments from the Eocene Arctic were provided by the Integrated Ocean Drilling Program (IODP). Financial support for this research was provided by the Darwin Center for Biogeosciences, the Royal NIOZ, and the University of Utrecht awarded (to J.S.S.D. and G.J.R.). G.J.R. acknowledges the Statoil Company for additional financial support.
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This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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