Rosko, J. | bioRxiv Science

bioRxiv2024

Cellular (de)coordination in gliding motility and plectoneme formation

2Cyanobacteria are key contributors to biogeochemical cycles through photosynthesis and carbon fixation. In filamentous, multicellular cyanobacteria these functions can be influenced through gliding motility, which enables filaments to localise in response to light and also form aggregates. Here, we use the aggregate forming species Fluctiforma draycotensis to study gliding motility dynamics in detail. We find that filaments move in curved and straight trajectories interspersed with re-orientation or reversal of direction. Most reversals take few seconds but some take substantially longer, resulting in a long-tailed distribution of stoppage times. Mean filament speeds range around a micron per second with a relatively uniform distribution against filament length, implying that all or fixed proportion of cells in a filament contribute to movement. We implement a biophysical model that can recapitulate these findings. Model simulations show that for filaments to reverse quickly, cells in a filament must achieve high coordination of the direction of the forces that they generate. To seek experimental support of this prediction, we track individual cells in a filament. This reveals that cells translational movement is fully coupled with their rotation along the long-axis of the filament, and that cellular movement remains coordinated throughout a reversal. For some filaments, especially longer ones, however, we also find that cellular coordination can be lost, and filaments can form buckles that can twist around themselves, resulting in plectonemes. The experimental findings and the biophysical model presented here will inform future studies of individual and collective filament movement. 1 Significance StatementCyanobacteria contribute to global oxygen production and carbon capture. Some cyanobacteria exist as multicellular filaments and display gliding motility that allows them to respond to light and to form aggregates, which influences their biological functions. Here, we study the dynamics of gliding motility. We find that filaments movement is interspersed with re-orientation or reversal of direction and that mean filament speed is mostly independent of filament length. We implement a biophysical model that predicts these features to relate to cells in a filament having high coordination of the direction of the forces that they generate. We find experimental support for this predicted cellular coordination, but also discover instances of longer filaments loosing coordination, resulting in buckling and entangling with other filaments.

biophysics↗

bioRxiv2022

Reproducible spatial structure formation and stable community composition in the cyanosphere predicts metabolic interactions

Understanding how microbial communities maintain stable compositional diversity is key for predicting community function. Studies from species pairwise interactions and synthetic communities indicate that metabolic interactions and spatial organisation can influence coexistence, but the relevance of these factors in more complex communities is unclear. Model systems often lack multi-species complexity, thereby making it difficult to study community diversity temporally. Here we used a spatially-organised cyanobacterial enrichment community to investigate compositional diversity and its stability. Over a year of passaging in media without significant carbon source, we found that the community maintains relatively high diversity, with 17 co-existing bacterial species. Using short and long read shotgun metagenomics sequencing from different time point samples, we have reconstructed complete genomes. Genomic annotation of these species revealed complementary metabolic functions involving carbon breakdown and vitamin biosynthesis suggesting interactions amongst community members. Using isolated species, we provide experimental support for carbon provision through cyanobacterial slime and growth on the component substrates by representative members of the Proteobacteria and Actinobacteriota phyla. Additionally, we experimentally show vitamin provision and uptake between prototrophic and auxotrophic members. We also found genomic capability for (an)oxygenic photosynthesis and sulfur cycling in several species. We show consistent formation of oxygen gradients across photogranule structures, supporting niches that can sustain these specific metabolic functions. These findings indicate that spatial niche formation and metabolic interactions enable maintenance of community compositional stability and diversity. SIGNIFICANCE STATEMENTMicrobes exist as species-diverse communities in nature and understanding their stability is an open challenge in microbial ecology. We established and maintained a spatially-organised, photosynthetic microbial community from a freshwater reservoir through long-term culturing in laboratory medium. We found that this community maintained a taxonomically-diverse set of 17 bacterial species. Combining genomic and physiological assays, we characterised a novel filamentous cyanobacterium capable of carbohydrate-rich slime secretion supporting growth of other microbes. We predict inter-species vitamin exchanges and identify sulfur cycling and alternative types of photosynthesis that are likely to be favoured in oxygen-free zones identified within the spatial structures. Our findings indicate that metabolic interactions and spatial structures can enable stable microbial coexistence in natural ecosystems.

microbiology↗