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

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

doi:10.1038/ncomms11071

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

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

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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.

Original language	English
Article number	11071
Journal	Nature Communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms11071
Publication status	Published - 22 Mar 2016
Externally published	Yes

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Cornejo-Castillo, F. M., Cabello, A. M., Salazar, G., Sánchez-Baracaldo, P., Lima-Mendez, G., Hingamp, P., Alberti, A., Sunagawa, S., Bork, P., De Vargas, C., Raes, J., Bowler, C., Wincker, P., Zehr, J. P., Gasol, J. M., Massana, R., & Acinas, S. G. (2016). Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton. Nature Communications, 7, Article 11071. https://doi.org/10.1038/ncomms11071

@article{7a5256192c5e4f43a0f10573a4448e4c,

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

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.",

author = "Cornejo-Castillo, {Francisco M.} and Cabello, {Ana M.} and Guillem Salazar and Patricia S{\'a}nchez-Baracaldo and Gipsi Lima-Mendez and Pascal Hingamp and Adriana Alberti and Shinichi Sunagawa and Peer Bork and {De Vargas}, Colomban and Jeroen Raes and Chris Bowler and Patrick Wincker and Zehr, {Jonathan P.} and Gasol, {Josep M.} and Ramon Massana and Acinas, {Silvia G.}",

year = "2016",

month = mar,

day = "22",

doi = "10.1038/ncomms11071",

language = "English",

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journal = "Nature Communications",

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Cornejo-Castillo, FM, Cabello, AM, Salazar, G, Sánchez-Baracaldo, P, Lima-Mendez, G, Hingamp, P, Alberti, A, Sunagawa, S, Bork, P, De Vargas, C, Raes, J, Bowler, C, Wincker, P, Zehr, JP, Gasol, JM, Massana, R & Acinas, SG 2016, 'Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton', Nature Communications, vol. 7, 11071. https://doi.org/10.1038/ncomms11071

TY - JOUR

T1 - Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton

AU - Cornejo-Castillo, Francisco M.

AU - Cabello, Ana M.

AU - Salazar, Guillem

AU - Sánchez-Baracaldo, Patricia

AU - Lima-Mendez, Gipsi

AU - Hingamp, Pascal

AU - Alberti, Adriana

AU - Sunagawa, Shinichi

AU - Bork, Peer

AU - De Vargas, Colomban

AU - Raes, Jeroen

AU - Bowler, Chris

AU - Wincker, Patrick

AU - Zehr, Jonathan P.

AU - Gasol, Josep M.

AU - Massana, Ramon

AU - Acinas, Silvia G.

PY - 2016/3/22

Y1 - 2016/3/22

N2 - 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.

AB - 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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U2 - 10.1038/ncomms11071

DO - 10.1038/ncomms11071

M3 - Article

C2 - 27002549

AN - SCOPUS:84961658202

SN - 2041-1723

VL - 7

JO - Nature Communications

JF - Nature Communications

M1 - 11071

ER -

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

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