Cyanobacteria and Chloroflexota cooperate to structure light-responsive biofilms

F Freddy Bunbury (Department of Ecology and Evolution, The University of Chicago) C Carlos Rivas (Department of Biosphere Sciences and Engineering, Carnegie Institution for Science) V Victoria Calatrava (Department of Biosphere Sciences and Engineering, Carnegie Institution for Science) A Andrey V. Malkovskiy (Department of Biosphere Sciences and Engineering, Carnegie Institution for Science) L Lydia-Marie Joubert (Division of CryoElectron Microscopy (CryoEM) and Bioimaging, Stanford Linear Accelerator Center (SLAC) National Accelerator Laboratory) A Amar D. Parvate (Environmental Molecular Sciences Division, Pacific Northwest National Laboratory) J James E. Evans (Environmental Molecular Sciences Division, Pacific Northwest National Laboratory) A Arthur R. Grossman (Department of Plant Biology, The Carnegie Institution for Science) D Devaki Bhaya (Department of Biosphere Sciences and Engineering, Carnegie Institution for Science)

Abstract

Microbial mats are stratified communities often dominated by unicellular and filamentous phototrophs within an exopolymer matrix. It is challenging to quantify the dynamic responses of community members in situ as they experience steep gradients and rapid fluctuations of light. To address this, we developed a binary consortium using two representative isolates from hot spring mats: the unicellular oxygenic phototrophic cyanobacterium Synechococcus OS-B′ (Syn OS-B′) and the filamentous anoxygenic phototroph Chloroflexus MS-CIW-1 (Chfl MS-1). We quantified the motility of individual cells and entire colonies and demonstrated that Chfl MS-1 formed bundles of filaments that moved in all directions with no directional bias to light. Syn OS-B′ was slightly less motile but exhibited positive phototaxis. This binary consortium displayed cooperative behavior by moving further than either species alone and formed ordered arrays where both species aligned with the light source. No cooperative motility was observed when a nonmotile pilB mutant of Syn OS-B′ was used instead of Syn OS-B′. The binary consortium also produced more adherent biofilm than individual species, consistent with the close interspecies association revealed by electron microscopy. We propose that cyanobacteria and Chloroflexota cooperate in forming natural microbial mats by colonizing new niches and building robust biofilms.

Article Details

Volume / Issue Vol. 122, Issue 5
Published February 04, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (9)

F

Freddy Bunbury

Department of Ecology and Evolution, The University of Chicago

C

Carlos Rivas

Department of Biosphere Sciences and Engineering, Carnegie Institution for Science

V

Victoria Calatrava

Department of Biosphere Sciences and Engineering, Carnegie Institution for Science

A

Andrey V. Malkovskiy

Department of Biosphere Sciences and Engineering, Carnegie Institution for Science

L

Lydia-Marie Joubert

Division of CryoElectron Microscopy (CryoEM) and Bioimaging, Stanford Linear Accelerator Center (SLAC) National Accelerator Laboratory

A

Amar D. Parvate

Environmental Molecular Sciences Division, Pacific Northwest National Laboratory

J

James E. Evans

Environmental Molecular Sciences Division, Pacific Northwest National Laboratory

A

Arthur R. Grossman

Department of Plant Biology, The Carnegie Institution for Science

D

Devaki Bhaya

Department of Biosphere Sciences and Engineering, Carnegie Institution for Science