Exploration of Social Spreading Reveals That This Behavior Is Prevalent among Pedobacter and Pseudomonas fluorescens Isolates and That There Are Variations in the Induction of the Phenotype

Appl Environ Microbiol. 2021 Sep 10;87(19):e0134421. doi: 10.1128/AEM.01344-21. Epub 2021 Jul 21.

Abstract

Within soil, bacteria are found in multispecies communities, where interactions can lead to emergent community properties. Studying bacteria in a social context is critical for investigating community-level functions. We previously showed that cocultured 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, the 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 Pseudomonas fluorescens Pf0-1 and Pedobacter sp. V48 interact, during which both species move together across a surface. Importantly, this environment does not permit the 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. Furthermore, we identify differences in mechanisms 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.

Keywords: Pedobacter; Pseudomonas fluorescens; emergent trait; interspecies interactions; motility; social motility.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Microbial Interactions*
  • Pedobacter / genetics
  • Pedobacter / physiology*
  • Phenotype
  • Phylogeny
  • Pseudomonas fluorescens / genetics
  • Pseudomonas fluorescens / physiology*
  • RNA, Ribosomal, 16S
  • Soil Microbiology

Substances

  • RNA, Ribosomal, 16S