Biology and genetic engineering of multicellular cyanobacteria

Enrique Flores, Antonia Herrero, Ignacio Luque, Rocío López-Igual, Laura Corrales-Guerrero and Mercedes Nieves-Morión

The Phylum Cyanobacteria includes species with a distinctive feature among prokaryotes: their capacity to perform oxygenic photosynthesis. Some species in this phylum also display phenomena such as multicellularity or cell differentiation, which are unusual among bacteria and make them considered instances of the highest complexity in the domain Bacteria. Multicellularity involves the aggregation and coordinated behavior of cells, which requires intercellular communication. Cyanobacteria of the order Nostocales such as Anabaena form filaments in which cells communicate by exchanging nutritional and signaling. Intercellular communication is the basis for phenomena that require the coordinated behavior of cells, such as establishing the differentiation pattern of heterocysts, which are cells specialized for the fixation of atmospheric nitrogen, or the synchronous circadian oscillation of multiple cells in the filament. Our group use multicellular cyanobacteria as models for investigation in several research lines that are described below.

1. Intercellular communication

Research leader: Enrique Flores

Heterocyst-forming cyanobacteria are multicellular organisms in which an exchange of nutrients and signaling molecules takes place between the cells of their filaments. We previously described the presence of a continuous periplasm along the cyanobacterial filament and of protein structures, termed septal junctions, that join the adjacent cells in the filament. In this topic, we are currently interested in the study of proteins that contribute to the formation and regulation of the septal junctions.

2. Cell division

Research leader: Antonia Herrero

In contrast to the separate daughters resulting from cell division in unicellular bacteria, cell division in multicellular cyanobacteria produce adjoined cells that are enclosed in a continuous outer membrane and connected by septal junctions, which are localized by the divisome. In addition, the heterocysts are terminally differentiated cells that have lost the capacity of cell division. We study the distinct features of cell division in Anabaena including a mechanism for inhibition of cell division during heterocyst differentiation.

3. Symbiosis

Research leaders: Mercedes Nieves-Morión, Enrique Flores

We aim at understanding some N2-fixing symbioses that are globally important in the Biosphere. For this, we study associations between diatoms and nitrogen-fixing cyanobacteria including heterocyst-forming cyanobacteria. We are especially interested in the mechanisms of nutrient exchange between the symbiotic partners.

4. Acclimation of the translation machinery to stress

Research leader: Ignacio Luque

The species of the order Nostocales dedicate a significant portion of their genome to acclimation functions. We are particularly interested in the mechanisms for acclimation to a variety of stress conditions, with emphasis on the role of the translation machinery. Currently, we are investigating the role of tRNAs, toxin-antitoxin systems, and RNA repair enzymes in the acclimation of Anabaena to stress. Additionally, we are exploring responses to various nutritional stress conditions, including metal deficiency.

5. Synthetic biology

Research leader: Rocío López-Igual

Cyanobacteria are attractive as potential factories for Biotechnology to produce, for instance, renewable energy sources. Major drawbacks for the proper development of these green factories are the instability of the cyanobacterial genome and the scarcity, when compared to heterotrophic systems, of genetic engineering tools. In this research line we combine the study of the genomic instability of Anabaena with the development of genetic tools for synthetic biology, with the aim of building cyanobacterial chases to be used for biotechnological applications.

6. Biomolecular condensates in cyanobacteria

Research leader: Laura Corrales-Guerrero

Biomolecular condensates (BMCs) are transient membraneless organelles which allow dynamic intracellular organization. This phenomenon is widespread in bacteria to perform different functions such as enhancing enzymatic activity, sequestration or cellular localization. The main scientific focus of this research line is: (1) to increase our knowledge about the molecular mechanisms governing BMC formation in cyanobacteria, and (2) to exploit their potential uses in biotechnology as enzymatic immobilization systems (in vitro or in vivo) and bioremediation.

Funding

Antonia Herrero

Proyecto P20-00032, Junta de Andalucía and FEDER.

Antonia Herrero, Enrique Flores:

Proyecto PID2020-118595GB-100 del MCIN/ AEI/10.13039/501100011033/

Enrique Flores

Proyecto PY20_00058, Junta de Andalucía and FEDER.

The Gordon and Betty Moore Foundation (USA), grant number 9355.

Rocío López-Igual:

Grant Ramón y Cajal: RYC2021-034768-I funded by MCIN/AEI/10.13039/501100011033 y EU “NextGenerationEU”/PRTR”.

Proyect: CNS2023-145397 funded by MCIN/AEI/10.13039/501100011033 y EU “NextGenerationEU”/PRTR”.

Proyect: PID2023-152188NB-I00 funded by MCIU/ AEI / 10.13039/501100011033 / FEDER, UE.

Ayudas Universidad de Sevilla: VI Plan Propio de Investigación y Transferencia de la Universidad de Sevilla, 2020; VII Plan Propio de Investigación y Transferencia de la Universidad de Sevilla, 2023. Ref: VIIPPIT-2023-II.2; Atracción Investigadores Alto Potencial. Ref: VIIPPIT-2022-II.5.

Ignacio Luque

Proyecto PID2021-128477NB-I00, MCIN/AEI/10.13039/501100011033/FEDER, UE.

Mercedes Nieves-Morión, Enrique Flores

Proyecto TED2021-130982B-I00, Agencia Estatal de Investigación, Ministerio de Ciencia e Innovación.

The Swedish Research Council (Sweden), grant number 2022-03319.

Laura Corrales-Guerrero

Contrato Ramón y Cajal: RYC2023-042841-I financiado por MCIU/AEI/ 10.13039/ 501100011033 y por el FSE+.

Proyecto PID2023-146704OA-I00 financiado por MCIU/ AEI / 10.13039/ 501100011033 / FEDER, UE, y contrato FPI financiado por MCIU/AEI/ 10.13039/ 501100011033 y por el FSE+.

Biología e ingeniería genética de cianobacterias multicelulares

NameSurnameCategoryemailPhones
Mª GraciaBenítez EslavaContracted on a project954489500
ext. 446093
MireiaBurnatPostdoctoral Contract954489500
ext. 446064
SergioCamargoPostdoctoral Researcher954489500
ext. 446092
LauraCorrales GuerreroUS Access Contract954489640
EnriqueFloresCSIC Research Professor954489523
AntoniaHerreroResearcher professor CSIC954489522
IgnacioLuqueCSIC Tenured Scientist954489633
RocíoLópez IgualRamón y Cajal Program Contract954489595
MercedesNieves MoriónPostdoctoral Contract954489500
ext. 446092
CristinaSarasa BuisánPostdoctoral Contract954489500
ext. 446092
AliciaSegura MejíasPredoctoral Fellowship954489500
ext. 446064
AnaValladaresSpecialized Higher Degree954489595
CristinaVelázquez-SuárezPostdoctoral Contract954489500
ext. 446093
MiguelÁngel RubioPostdoctoral Researcher954489500
ext. 446092

  • Angulo-Cánovas E, Bartual A, López-Igual R, Luque I, Radzinski NP, Shilova I, Anjur-Dietrich M, García-Jurado G, Úbeda B, González-Reyes JA, Díez J, Chisholm SW, García-Fernández JM, Muñoz-Marín MdC (2024) Direct interaction between marine cyanobacteria mediated by nanotubes. Sci Adv. 10:eadj1539. doi: 10.1126/sciadv.adj1539. 

 

  • Arbel-Goren R, Dassa B, Zhitnitsky A, Valladares A, Herrero A, Flores E, Stavans J (2024) Spatio-temporal coherence of circadian clocks and temporal control of differentiation in Anabaena filaments. mSystems 9(1):e0070023. doi: 10.1128/msystems.00700-23.

 

  • Sarasa-Buisan C, Nieves-Morión M, Arévalo S, Helm RF, Sevilla E, Luque I, Fillat MF (2024) FurC (PerR) contributes to the regulation of peptidoglycan remodeling and intercellular molecular transfer in the cyanobacterium Anabaena sp. strain PCC 7120. mBio 15(3):e0323123. doi: 10.1128/mbio.03231-23.

 

 

  • Sarasa-Buisan C, Ochoa de Alda JAG, Velázquez-Suárez C, Rubio MÁ, Gómez-Baena G, Fillat MF, Luque I (2024) An ancient bacterial zinc acquisition system identified from a cyanobacterial exoproteome. PLoS Biol 22(3):e3002546. doi: 10.1371/journal.pbio.3002546.
  • López-Igual R, Dorado-Morales P, Mazel D (2023) Increasing the scalability of toxin-intein orthogonal combinations. ACS Synth Biol 12(2):618-623. doi: 10.1021/acssynbio.2c00477.
  • Nieves-Morión M, Camargo S, Bardi S, Ruiz MT, Flores E, Foster RA (2023) Heterologous expression of genes from a cyanobacterial endosymbiont highlights substrate exchanges with its diatom host. PNAS Nexus 2(6), pgad194/7205781. doi: org/10.1093/pnasnexus/pgad194.
  • Valladares A, Picossi S, Corrales-Guerrero L, Herrero A (2023) The role of SepF in cell division and diazotrophic growth in the multicellular cyanobacterium Anabaena sp. strain PCC 7120. Microbiol Res 277: 127489. doi: 10.1016/j.micres.2023.127489. 

 

 

  • Velázquez-Suárez C, Springstein B, Nieves-Morión M, Helbig AO, Kieninger AK, Maldener I, Nürnberg DJ, Stucken K, Luque I, Dagan T, Herrero A (2023) SepT, a novel protein specific to multicellular cyanobacteria, influences peptidoglycan growth and septal nanopore formation in Anabaena sp. PCC 7120. mBio 14(5):e0098323. doi:10.1128/mbio.00983-23.
  • Funck D, Sinn M, Fleming J, Stanoppi M, Dietrich J, López-Igual R, Mayans O, and Hartig JS (2022) Discovery of a Ni(II)-dependent guanidine hydrolase in bacteria. Nature 603:515-521. doi: 10.1038/s41586-022-04490-x.

 

 

  • Velázquez-Suárez C, Valladares A, Luque I, Herrero A (2022) The Role of Mre Factors and Cell Division in Peptidoglycan Growth in the Multicellular Cyanobacterium Anabaena. mBio 13(4):e0116522. doi: 10.1128/mbio.01165-22. 

 

 

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