Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton

© Nils Lola Reboud

Tara Oceans

Francisco M. Cornejo-Castillo, Ana M. Cabello, Guillem Salazar, Patricia Sánchez-Baracaldo, Gipsi Lima-Mendez, Pascal Hingamp, Adriana Alberti, Shinichi Sunagawa, Peer Bork, Colomban de Vargas, Jeroen Raes, Chris Bowler, Patrick Wincker, Jonathan P. Zehr, Josep M. Gasol, Ramon Massana & Silvia G. Acinas

Nature Communications 7,
Article number: 11071 (2016)
doi:10.1038/ncomms11071
Published online: 22 March 2016

Researchers from the Spanish National Research Council – CSIC (Spain), alongside colleagues from several international institutions, have delved into the characterization of an unusual relationship between marine planktonic microorganisms involved in the marine nitrogen cycle. This longstanding relationship evolved 90 million years ago in the Cretaceous at a time when the Earth oceans were nutrient deprived.

This study, which used data from the Tara Oceans expedition and partially realised in the framework of OCEANOMICS, is published in Nature Communications

Press release

Nitrogen is an essential component of the amino acids that make up proteins and of nucleic acids like DNA. However, whilst nitrogen is hugely abundant in the atmosphere (up to 80%), most organisms can’t breathe nitrogen; they rely on bacteria to take it from the atmosphere and transform it into bioavailable nitrogen that other organisms of the marine food web can use. Thus, oceanic primary productivity would not occur without these nitrogen-fixing bacteria. A group of photosynthetic bacteria known as cyanobacteria are among the microbes displaying this capability.

Very recently a bizarre cyanobacterium has been discovered – a unicellular nitrogen fixer crippled in its photosynthetic capabilities and that was enslaved by a more complex host cell. The new findings have revealed that the sole purpose of this cyanobacterium, called UCYN-A, is to provide nitrogen to its host, a single-celled prymnesiophyte alga, and this ‘enslaving event’ occurred around 90 million years ago, towards the end of the Cretaceous, just after a paleo-oceanographic context in which the lowest nutrient regime of the last 500 million years occurred.

« The obligatory nature of this symbiosis together with the genome reduction suffered by UCYN-A and the expression of their genome content, mainly focused on nitrogen fixation, suggest that we are facing a similar evolutionary process that led to chloroplasts in plants, that is the formation of an organelle of bacterial origin whose function is to provide nitrogen to its host » explains the first author of the study, Francisco M. Cornejo-Castillo (CSIC, Spain).

The study, with implications in evolutionary biology, describes two symbiotic partnerships formed by two ‘sister’ UCYN-A species and two ‘sister’ prymnesiophyte species, which apparently evolved in parallel. This work provides epifluorescence microscopy images that show the specificity of the two symbiotic systems in which the partner fidelity by each symbiotic pair is demonstrated. The hosting cells, the two prymnesiophyte species, could have acted as a physical barrier isolating the cyanobacterial ancestor of the UCYN-A symbionts and originating new UCYN-A species.

Dr Silvia G. Acinas, from ICM-CSIC in Spain, who led the study, said: « This is a very important symbiotic system in marine environments because they are globally distributed, playing a significant role in nitrogen and carbon marine cycles.»

This research has been made possible thanks to the metagenome and metatranscriptome datasets obtained from the Tara Oceans oceanographic expedition.

Several international laboratories including the University of Bristol (UK), VIB/VUB/KU Leuven (Belgium), Aix-Marseille Université (France), Centre National de la Recherche Scientifique – CNRS (France), Genoscope (France), European Molecular Biology Laboratory – EMBL (Germany) and the University of California (USA) participated in this study.

 

Abstract

The unicellular cyanobacterium UCYN-A, one of the major contributors to nitrogen fixation in the open ocean, lives in symbiosis with single-celled phytoplankton. UCYN-A includes several closely related lineages whose partner fidelity, genome-wide expression and time of evolutionary divergence remain to be resolved. Here we detect and distinguish UCYN-A1 and UCYN-A2 lineages in symbiosis with two distinct prymnesiophyte partners in the South Atlantic Ocean. Both symbiotic systems are lineage specific and differ in the number of UCYN-A cells involved. Our analyses infer a streamlined genome expression towards nitrogen fixation in both UCYN-A lineages. Comparative genomics reveal a strong purifying selection in UCYN-A1 and UCYN-A2 with a diversification process ∼91 Myr ago, in the late Cretaceous, after the low-nutrient regime period occurred during the Jurassic. These findings suggest that UCYN-A diversified in a co-evolutionary process, wherein their prymnesiophyte partners acted as a barrier driving an allopatric speciation of extant UCYN-A lineages.

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