Microbial Interactions in Oral Communities Mediate Emergent Biofilm Properties

Oral microbial communities are extraordinarily complex in taxonomic composition and comprise interdependent biological systems. The bacteria, archaea, fungi, and viruses that thrive within these communities engage in extensive cell-cell interactions, which are both beneficial and antagonistic. Direct physical interactions among individual cells mediate large-scale architectural biofilm arrangements and provide spatial proximity for chemical communication and metabolic cooperation. In this review, we summarize recent work in identifying specific molecular components that mediate cell-cell interactions and describe metabolic interactions, such as cross-feeding and exchange of electron acceptors and small molecules, that modify the growth and virulence of individual species. We argue, however, that although pairwise interaction models have provided useful information, complex community-like systems are needed to study the properties of oral communities. The networks of multiple synergistic and antagonistic interactions within oral biofilms give rise to the emergent properties of persistence, stability, and long-range spatial structure, with these properties mediating the dysbiotic transitions from health to oral diseases. A better understanding of the fundamental properties of interspecies networks will lead to the development of effective strategies to manipulate oral communities.

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Exploration of social spreading reveals behavior is prevalent among Pedobacter and P. fluorescens isolates, and shows variations in induction of phenotype

Applied and Environmental Microbiology ◽

10.1128/aem.01344-21 ◽

2021 ◽

Author(s):

Lucy M. McCully ◽

Jasmine Graslie ◽

Alana R. McGraw ◽

Adam S. Bitzer ◽

Auður M. Sigurbjörnsdóttir ◽

...

Keyword(s):

Microbial Communities ◽

Close Contact ◽

Soil Microbial Communities ◽

Group Behavior ◽

Microbial Interactions ◽

Emergent Behavior ◽

Individual Species ◽

Emergent Properties ◽

Community Function ◽

The Individual

Within soil, bacteria are found in multi-species communities, where interactions can lead to emergent community properties. Studying bacteria in a social context is critical for investigation of community-level functions. We previously showed that co-cultured Pseudomonas fluorescens Pf0-1 and Pedobacter sp. V48 engage in interspecies social spreading (ISS) on a hard agar surface, a behavior which required close contact and depended on the nutritional environment. Here, we investigate whether social spreading is widespread among P. fluorescens and Pedobacter isolates, and whether the requirements for interaction vary. We find that this phenotype is not restricted to the interaction between P. fluorescens Pf0-1 and Pedobacter sp. V48, but is a prevalent behavior found in one clade in the P. fluorescens group and two clades in the Pedobacter genus. We show that the interaction with certain Pedobacter isolates occurred without close contact, indicating induction of spreading by a putative diffusible signal. As with ISS by Pf0-1+V48, motility of interacting pairs is influenced by the environment, with no spreading behaviors (or induction of motility) observed under high nutrient conditions. While Pf0-1+V48 require low nutrient but high NaCl conditions, in the broader range of interacting pairs the high salt influence was variable. The prevalence of motility phenotypes observed here and found within the literature indicates that community-induced locomotion in general, and social spreading in particular, is likely important within the environment. It is crucial that we continue to study microbial interactions and their emergent properties to gain a fuller understanding of the functions of microbial communities. Importance Interspecies social spreading (ISS) is an emergent behavior observed when P. fluorescens Pf0-1 and Pedobacter sp. V48 interact, during which both species move together across a surface. Importantly, this environment does not permit movement of either individual species. This group behavior suggests that communities of microbes can function in ways not predictable by knowledge of the individual members. Here we have asked whether ISS is widespread and thus potentially of importance in soil microbial communities. The significance of this research is the demonstration that surface spreading behaviors are not unique to the Pf0-1-V48 interaction, but rather is a more widespread phenomenon observed among members of distinct clades of both P. fluorescens and Pedobacter isolates. Further, we identify differences in mechanism of signaling and nutritional requirements for ISS. Emergent traits resulting from bacterial interactions are widespread and their characterization is necessary for a complete understanding of microbial community function.

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