Fossilized glycolipids reveal past oceanic N ₂ fixation by heterocystous cyanobacteria

Abstract

N 2 -fixing cyanobacteria play an essential role in sustaining primary productivity in contemporary oceans and freshwater systems. However, the significance of N 2 -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 N 2 -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 N 2 -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.nitrogen fixation | intact polar lipids | cyanobacterial biomarkers | symbiosis | saproprel

Geomicrobial functional groups: A window on the interaction between life and environments

“…Nitrogen isotopic fractionation during nitrogen-fixation and non nitrogen-fixation has been discriminated clearly in supratidal and intertidal microbial mats. Organic nitrogen isotope composition was clearly more negative in supratidal than in intertidal microbial mats, and heterocyst glycolipids, the biomarkers of some nitrogen-fixing cyanobacteria, were identified only in supratidal microbial mats [78]. The negative shifts of δ 15 N during Cretaceous oceanic anoxic events and across the PermianTriassic boundary both indicate past blooms of cyanobacteria [129,130], consistent with the occurrence of enhanced cyanobacterial biomarkers [131].…”

“…After molecular oxygen accumulated in the atmosphere and oceans, the nitrogen-fixing microbes were able to develop a number of special strategies (e.g. heterocyst and photosystem I) to separate nitrogenase from free oxygen [78]. In the early evolution of Earth, the scarcity of nitrate and ammonium may have triggered a selection pressure, favoring the evolution of nitrogenase in anaerobic microorganisms (e.g.…”

“…glycolipids in heterocysts), which can protect the O 2 -sensitive nitrogenase from inactivation. The heterocyst glycolipids can be preserved in sediments for a long time because of their resistance to degradation, and can be used as biomarkers to trace nitrogen-fixation cyanobacteria in ancient oceans [78]. Specific unsaturated bacteriohopanepolyols with four hydroxyl side chains are diagnostic of nitrogen-fixing cyanobacteria, Trichodesmium, the dominant microbes in modern oceans [123].…”

Late Cretaceous seasonal palaeoclimatology and diatom palaeoecology from laminated sediments

“…In all these cases, Hemiaulus blooms are, in part, fuelled by a non-obligate symbiosis with the nitrogen fixing cyanobacterial symbiont Richelia intracellularis in Diatom Diazotroph Associations (DDAs). Laminae of Hemiaulus hauckii are also a component of the Mediterranean sapropels and there is biomarker evidence of the abundant presence of N 2 -fixing cyanobacteria during sapropel formation (Bauersachs et al, 2010). Although there is no direct evidence from the Cretaceous, there is widespread isotopic evidence for contemporaneous N-fixation (Meyers et al, 2009) In summary, Upper Cretaceous sequences demonstrate substantial growth of Hemiaulus spp.…”

Comparison of extraction and work up techniques for analysis of core and intact polar tetraether lipids from sedimentary environments

“…Huguet et al, 2010a). However, it has been reported that ASE at 100 °C and 20 kPa is capable of quantitatively extracting glycolipids from heterocystous cyanobacteria (Bauersachs et al, 2010), so we re-investigated its potential for extracting archaeal IPLs. IPL quantification was carried out by way of separation over SiO 2 , followed by acid hydrolysis, according to Pitcher et al (2009b), and by direct hydrolysis according to Huguet et al (2010a).…”