Niche formation and metabolic interactions result in stable diversity in a spatially structured cyanobacterial community

Abstract

Cyanobacterial granules and aggregates can readily form in aquatic environments. The microbial communities found within and around these structures can be referred to as the cyanosphere, and can enable collective metabolic activities relevant to biogeochemical cycles. Cyanosphere communities are suggested to have different composition to that in the surrounding environment, but studies to date are mostly based on single time point samples. Here, we retrieved samples containing cyanobacterial granules from a freshwater reservoir and maintained a culture through sub-culture passages under laboratory conditions for over a year. We show that cyanobacteria-dominated granules form readily and repeatedly in this system over passages, and that this structure formation process seems to be associated with cyanobacterial motility. Performing longitudinal short-read sequencing over several culture passages, we identified a cyanosphere community comprising of 17 species with maintained population structure. Using long-read sequencing from two different time point samples, we have re-constructed full, circular genomes for 15 of these species and annotated metabolic functions within. This predicts several metabolic interactions among community members, including sulfur cycling and carbon and vitamin exchange. Using three individual species isolated from this cyanosphere, we provide experimental support for growth on carbon sources predicted to be secreted by the cyanobacterium in the system. These findings reinforce the view that the cyanosphere can recruit and maintain a specific microbial community with specific functionalities embedded in a spatially-organised microenvironment. The presented community will act as a key model system for further understanding the formation of the structured cyanosphere, its function and stability, and its metabolic contribution to biogeochemical cycles.

Formation and emergent dynamics of spatially organized microbial systems

“…In some of these cases, the exact temporal dynamics and mechanistic processes leading to spatial organization are still unclear. In the case of phototrophic granules, the presence of motile, filamentous cyanobacteria has been highlighted as an important feature [ 2 , 39 , 42 ]. Some cyanobacteria are readily found to exist in aggregate colonies in nature [ 6 , 39 , 41 ], and can form aggregate structures under laboratory conditions [ 2 , 39 ].…”

“…In the case of phototrophic granules, the presence of motile, filamentous cyanobacteria has been highlighted as an important feature [ 2 , 39 , 42 ]. Some cyanobacteria are readily found to exist in aggregate colonies in nature [ 6 , 39 , 41 ], and can form aggregate structures under laboratory conditions [ 2 , 39 ]. Several cyanobacteria are known to secrete a range of extracellular polymers, often referred to as ‘mucus’, facilitating their gliding motility [ 45 , 46 ], and these can enhance aggregation.…”

“…It is, therefore, plausible that aqueous environments may readily result in physically driven initial aggregation of certain microorganisms ( figure 1 a ), which can then lead to formation of larger granules through random colonization or recruitment of select bacteria from the environment ( figure 1 b ) [ 2 , 6 , 39 ]. The granules may sink and become seed for a new biofilm [ 48 ].…”

“…There is still a lot unknown about the exact physical processes and population dynamics of initial formation and subsequent development of SOMS. There are, however, emerging model systems from bioreactors [ 2 , 44 , 68 ], open ocean [ 69 ] and freshwater environments [ 39 ], which might allow these questions to be tractably addressed in the future.…”

“…This is a form of self-organization, whereby cell movement, attachment and interaction can lead to segregation, pattern formation or collective motion of cells with examples seen already in model systems of single-species biofilms [4,5,[28][29][30]. In the case of multispecies natural communities, microbial aggregates and granules are found to emerge in aquatic environments, including the open ocean, and in bioreactors [2,6,[38][39][40][41][42][43][44]. In some of these cases, the exact temporal dynamics and mechanistic processes leading to spatial organization are still unclear.…”