Surface sensing stimulates cellular differentiation in Caulobacter crescentus

Abstract

Cellular differentiation is a fundamental strategy used by cells to generate specialized functions at specific stages of development. The bacterium Caulobacter crescentus employs a specialized dimorphic life cycle consisting of two differentiated cell types. How environmental cues, including mechanical inputs such as contact with a surface, regulate this cell cycle remain unclear. Here, we find that surface sensing by the physical perturbation of retracting extracellular pilus filaments accelerates cell-cycle progression and cellular differentiation. We show that physical obstruction of dynamic pilus activity by chemical perturbation or by a mutation in the outer-membrane pilus secretin CpaC stimulates early initiation of chromosome replication. In addition, we find that surface contact stimulates cell-cycle progression by demonstrating that surface-stimulated cells initiate early chromosome replication to the same extent as planktonic cells with obstructed pilus activity. Finally, we show that obstruction of pilus retraction stimulates the synthesis of the cell-cycle regulator cyclic diguanylate monophosphate (c-di-GMP) through changes in the activity and localization of two key regulatory histidine kinases that control cell fate and differentiation. Together, these results demonstrate that surface contact and sensing by alterations in pilus activity stimulate C. crescentus to bypass its developmentally programmed temporal delay in cell differentiation to more quickly adapt to a surface-associated lifestyle.

Nutrient complexity triggers transitions between solitary and colonial growth in bacterial populations

“…Our work uses a well-studied genetic model system to study growth on natural substrates and thus provides a basis to extend mechanistic studies in the context of the natural ecology of bacteria. It is known that cellular appendages like pili and holdfast adhesins allow C. crescentus cells to colonize surfaces [ 41 , 42 ] and thus are likely involved in colony formation on xylan. In contrast, flagella allow cells to swim.…”

Mimicking biofilm formation and development: Recent progress in in vitro and in vivo biofilm models

“…Moreover, at this point, bacteria not only become prepared to mount an adequate response for themselves or neighboring cells during the adsorption and adhesion stages but also has been reported that bacteria are able to “keep track” of these events retaining a multigenerational memory through the oscillations in the levels of the second messenger molecule cyclic adenosine 3′,5′-monophosphate (cAMP) and type IV pili activity ( Lee et al., 2018 ). Finally, it has been recently reported that the biofilm forming environmental bacteria C. crescentus experience cell differentiation and speed up cell cycle progression after surface sensing ( Snyder et al., 2020 ).…”

c-di-GMP Homeostasis Is Critical for Heterocyst Development in Anabaena sp. PCC 7120

“…It was first discovered in Gluconacetobacter xylinus about 30years ago, as a positive allosteric regulator of cellulose synthase ( Ross et al, 1987 ). Subsequent studies have revealed that c-di-GMP regulates a variety of important cellular processes, including biofilm formation, motility, virulence, cell differentiation, cell cycle and mechanical sensing ( Tischler and Camilli, 2004 ; Kulesekara et al, 2006 ; Hengge, 2009 ; Boehm et al, 2010 ; Romling et al, 2013 ; Tschowri et al, 2014 ; Lori et al, 2015 ; Hug et al, 2017 ; Xu et al, 2019 ; Del Medico et al, 2020 ; Snyder et al, 2020 ). Such regulations may take place at the transcriptional, post-transcriptional, or post-translational levels by interacting with different types of effectors ( Romling et al, 2013 ; Chou and Galperin, 2016 ).…”