Impact of direct physical association and motility on fitness of a synthetic interkingdom microbial community

Abstract

Mutualistic exchange of metabolites can play an important role in microbial communities. Under natural environmental conditions, such exchange may be compromised by the dispersal of metabolites and by the presence of non-cooperating microorganisms. Spatial proximity between members during sessile growth on solid surfaces has been shown to promote stabilization of cross-feeding communities against these challenges. Nonetheless, many natural cross-feeding communities are not sessile but rather pelagic and exist in turbulent aquatic environments, where partner proximity is often achieved via direct cell-cell adhesion, and cooperation occurs between physically associated cells. Partner association in aquatic environments could be further enhanced by motility of individual planktonic microorganisms. In this work, we establish a model bipartite cross-feeding community between bacteria and yeast auxotrophs to investigate the impact of direct adhesion between prokaryotic and eukaryotic partners and of bacterial motility in a stirred mutualistic co-culture. We demonstrate that adhesion can provide fitness benefit to the bacterial partner, likely by enabling local metabolite exchange within co-aggregates, and that it counteracts invasion of the community by a non-cooperating cheater strain. In a turbulent environment and at low cell densities, fitness of the bacterial partner and its competitiveness against a non-cooperating strain are further increased by motility that likely facilitates partner encounters and adhesion. These results suggest that, despite their potential fitness costs, direct adhesion between partners and its enhancement by motility may play key roles as stabilization factors for metabolic communities in turbulent aquatic environments.

Tuning Interdomain Conjugation Towardin situPopulation Modification in Yeast

“…Fluorescence microscopy analysis replicated previous findings 50 showing that adding mannose to growth media prevented most bacteria-yeast clumping (Fig 3a). Image analysis demonstrated that the size of yeast clumps—a proxy for number of yeast cells per clump—increased concurrent with the number of bacteria in a clump (“coincident bacteria”), implying that bacteria mediate cell clump formation (SF5, SF6).…”

“…Since IDC depends on cell-cell collisions in culture, we explored how known adherence mechanisms between E. coli and S. cerevisiae affect IDC. Mannoproteins are ubiquitous in fungal cell walls 57 , and type I fimbriae in E. coli bind to these 58,59 , forming bacteria-yeast “clumps” that can affect crossfeeding dynamics 50 . We thus repeated our batch culture experiments for population dynamics and IDC with- and without mannose added to the media, which saturates bacterial mannose receptors and reduces clumping.…”

Cross-Feeding between Filamentous Cyanobacteria and Symbiotic Bacteria Favors Rapid Photogranulation

“…Close spatial proximity is essential for effective cross-feeding, and the acquisition of metabolites is a key factor for aggregate formation . Although metabolites are highly dispersible and equally distributed in well-mixed environments, , some costly metabolites (i.e., vitamins, amino acids) of FC might be instantly consumed by the surrounding bacteria. To obtain access to valuable phytoplankton products, some bacteria actively move to the phytoplankton surface. ,, This is consistent with the enhanced expression of chemotaxis and flagellar assembly-related genes of symbiotic bacteria with motility (PRO1 and PRO5) in Rf (Figure S11).…”

Metabolite Cross-Feeding Promoting NADH Production and Electron Transfer during Efficient SMX Biodegradation by a Denitrifier and S. oneidensis MR-1 in the Presence of Nitrate

“…11,15,16 For example, in a model bipartite cross-feeding community between bacteria and yeast auxotrophs, flagella mediated the adhesion of two microorganisms to promote local metabolite exchange within the coaggregates, providing fitness benefits to bacterial partners, and counteracted the invasion of the community by uncooperative deceptive strains. 17 By constructing a metabolic model, A. R. Pacheco et al found that costless metabolite cross-feeding enhanced growth capacities, offset nutrients competition, and produced stable interaction motifs. 11 It seems that using two or more microorganisms to treat multiple pollutants will achieve a better performance than a sole microorganism.…”

“…As we all know, microorganisms usually exist in the environment in the form of coexistence with other ones, and each microbe obtains its own favorable niche through interspecific communication and interaction. − When encountering some external pressure (e.g., the presence of pollutants or unfavorable growth or metabolic conditions), different microorganisms in the environment often cooperate with each other to improve the pressure situation by reducing the metabolic burden and increasing tolerance to environmental challenges through inherent trade-offs, such as division of labor and resource exchange. ,, For example, in a model bipartite cross-feeding community between bacteria and yeast auxotrophs, flagella mediated the adhesion of two microorganisms to promote local metabolite exchange within the coaggregates, providing fitness benefits to bacterial partners, and counteracted the invasion of the community by uncooperative deceptive strains . By constructing a metabolic model, A. R. Pacheco et al found that costless metabolite cross-feeding enhanced growth capacities, offset nutrients competition, and produced stable interaction motifs .…”