Diversity in Starvation Survival Strategies and Outcomes among Heterotrophic Proteobacteria

Abstract

Heterotrophic Proteobacteria are versatile opportunists that have been extensively studied as model organisms in the laboratory, as both pathogens and beneficial symbionts of plants and animals, and as ubiquitous organisms found free-living in many environments. Succeeding in these niches requires an ability to persist for potentially long periods of time in growth-arrested states when essential nutrients become limiting. The tendency of these bacteria to grow in dense biofilm communities frequently leads to the development of steep nutrient gradients and deprivation of interior cells even when the environment is nutrient rich. Surviving within host environments also likely requires tolerating growth arrest due to the host limiting access to nutrients and transitioning between hosts may require a period of survival in a nutrient-poor environment. Interventions to maximise plant-beneficial activities and minimise infections by bacteria will require a better understanding of metabolic and regulatory networks that contribute to starvation survival, and how these networks function in diverse organisms. Here we focus on carbon starvation as a growth-arresting condition that limits availability not only of substrates for biosynthesis but also of energy for ongoing maintenance of the electrochemical gradient across the cell envelope and cellular integrity. We first review models for studying bacterial starvation and known strategies that contribute to starvation survival<i>.</i> We then present the results of a survey of carbon starvation survival strategies and outcomes in ten bacterial strains, including representatives from the orders Enterobacterales and Pseudomonadales (both Gammaproteobacteria) and Burkholderiales (Betaproteobacteria). Finally, we examine differences in gene content between the highest and lowest survivors to identify metabolic and regulatory adaptations that may contribute to differences in starvation survival.

Search for a Shared Genetic or Biochemical Basis for Biofilm Tolerance to Antibiotics across Bacterial Species

“…This preliminary finding supports the hypothesis that all three biofilms experience restriction of growth and express some stationary-phase character. The gene sets for each of the three microorganisms, however, display little specific or functional overlap (68).…”

ATP is a major determinant of phototrophic bacterial longevity in growth arrest

“…In E. coli , hibernating ribosomes account for only about 60% of the total ribosome pool in stationary phase cells (25) and although E. coli has other mechanisms to shut down protein synthesis (26, 27), it is unclear whether it does so completely. Certainly, there is evidence that growth-arrested cells of E. coli and other gram-negative bacteria continue to synthesize proteins for days (4, 28). This suggests that some heterotrophic bacteria in growth arrest may resemble energy-replete growth-arrested R. palustris in prioritizing protein synthesis as a survival strategy.…”

“…Growth arrest can be caused by many factors including starvation for carbon, nitrogen, phosphate, or other nutrients that cells need for growth and replication. Many nutrients exist in growth-limiting amounts in natural environments (2), and bacteria can survive for long periods of time when growing very slowly or not at all (3)(4)(5). There are practical reasons to better understand the physiology of non-growing bacteria.…”

Functional and Seasonal Changes in the Structure of Microbiome Inhabiting Bottom Sediments of a Pond Intended for Ecological King Carp Farming

“…The analysis of the bacterial structure at the phylum level revealed the dominance of Proteobacteria inhabiting the bottom sediments in a large abundance (15–70%) in all seasons of the year, with prevalence in spring ( Figure 3 ) at all sampling points in Cardinal Pond ( Figure 2 ). Here, it is worth noting that Proteobacteria are heterotrophic, versatile opportunists and have been extensively studied not only as both pathogens and beneficial symbionts of plants and animals, but also as ubiquitous organisms that live freely (autochthonously) in many environments [ 25 ]. In addition, they find potential applications in biotechnology as iron-oxidizing bacteria [ 26 ] and have an underestimated potential to produce bioactive molecules [ 27 ]; therefore, their presence in bottom sediment seems to be desirable.…”