α-cyanobacteria possessing form IA RuBisCO globally dominate aquatic habitats

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Abstract

RuBisCO (ribulose 1,5-bisphosphate carboxylase/oxygenase) is one the most abundant enzymes on Earth. Virtually all food webs depend on its activity to supply fixed carbon. In aerobic environments, RuBisCO struggles to distinguish efficiently between CO2 and O2. To compensate, organisms have evolved convergent solutions to concentrate CO2 around the active site. The genetic engineering of such inorganic carbon concentrating mechanisms (CCMs) into plants could help facilitate future global food security for humankind. In bacteria, the carboxysome represents one such CCM component, of which two independent forms exist: α and β. Cyanobacteria are important players in the planet’s carbon cycle and the vast majority of the phylum possess a β-carboxysome, including most cyanobacteria used as laboratory models. The exceptions are the exclusively marine Prochlorococcus and Synechococcus that numerically dominate open ocean systems. However, the reason why marine systems favor an α-form is currently unknown. Here, we report the genomes of 58 cyanobacteria, closely related to marine Synechococcus that were isolated from freshwater lakes across the globe. We find all these isolates possess α-carboxysomes accompanied by a form 1A RuBisCO. Moreover, we demonstrate α-cyanobacteria dominate freshwater lakes worldwide. Hence, the paradigm of a separation in carboxysome type across the salinity divide does not hold true, and instead the α-form dominates all aquatic systems. We thus question the relevance of β-cyanobacteria as models for aquatic systems at large and pose a hypothesis for the reason for the success of the α-form in nature.

Item Type: Journal Article
Subjects: Q Science > QR Microbiology
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Cyanobacteria, Water -- Microbiology, Microbial ecology
Journal or Publication Title: The ISME Journal
Publisher: Nature Publishing Group
ISSN: 1751-7362
Official Date: October 2022
Dates:
Date
Event
October 2022
Published
18 July 2022
Available
28 June 2022
Accepted
25 January 2022
Submitted
Volume: 16
Page Range: pp. 2421-2432
DOI: 10.1038/s41396-022-01282-z
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons open licence)
Date of first compliant deposit: 2 August 2022
Date of first compliant Open Access: 3 August 2022
RIOXX Funder/Project Grant:
Project/Grant ID
RIOXX Funder Name
Funder ID
NE/N003241/1
[NERC] Natural Environment Research Council
883551
[ERC] Horizon 2020 Framework Programme
APOSTD/2019/009
Generalitat Valenciana
CGL2016-76273-P
Ministerio de Ciencia e Innovación
PID2019-104742RB-I00
Ministerio de Ciencia e Innovación
PROMETEO/2019/009
Generalitat Valenciana
UNSPECIFIED
[MES] Ministry of Education and Science of the Russian Federation
URI: https://wrap.warwick.ac.uk/167805/

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