Is biofilm formation intrinsic to the origin of life?

Abstract

Biofilms are multicellular, often surface‐associated, communities of autonomous cells. Their formation is the natural mode of growth of up to 80% of microorganisms living on this planet. Biofilms refractory towards antimicrobial agents and the actions of the immune system due to their tolerance against multiple environmental stresses. But how did biofilm formation arise? Here, I argue that the biofilm lifestyle has its foundation already in the fundamental, surface‐triggered chemical reactions and energy preserving mechanisms that enabled the development of life on earth. Subsequently, prototypical biofilm formation has evolved and diversified concomitantly in composition, cell morphology and regulation with the expansion of prokaryotic organisms and their radiation by occupation of diverse ecological niches. This ancient origin of biofilm formation thus mirrors the harnessing environmental conditions that have been the rule rather than the exception in microbial life. The subsequent emergence of the association of microbes, including recent human pathogens, with higher organisms can be considered as the entry into a nutritional and largely stress‐protecting heaven. Nevertheless, basic mechanisms of biofilm formation have surprisingly been conserved and refunctionalized to promote sustained survival in new environments.

Evolution of cyclic di-GMP signalling on a short and long term time scale

“…We assume that first GGDEF domains exclusively possessed catalytic activity as predicted for proteins found in members of the deepest branching phyla [17] and enzymatic inactivation of cyclic di-GMP turnover proteins to be a secondary event. An example of the subsequent loss of catalytic activity of cyclic di-GMP turnover proteins with development to be directly connected to biological relevance is provided in the evolution of the enteric pathogen Yersinia pseudotuberculosis to the flea-born pathogen Yersinia pestis [43, 44].…”

“…Few protein receptor binding sites possess an affinity in the nanomolar range equally as most cyclic di-nucleotide binding RNA aptamers, while most protein receptor binding site have a 100 to 1000-fold lower affinity in the µM range [15,16]. In concurrence with its ancient phylogenetic origin and abundance [17], cyclic di-GMP signalling affects molecular mechanisms from modulating the binding properties of transcription factors to regulation of enzymatic activities and protein-protein interactions. Thereby, fundamental microbial physiological and metabolic processes can be affected which span from the oxidation of Mn 2+ , a process that is required for water clearance, the differential use of carbon sources and differential biofilm formation in host cells to the role of cyclic di-GMP as an extracellular signalling molecule [18][19][20][21].…”

Architecture, Function, Regulation, and Evolution of α-Glucans Metabolic Enzymes in Prokaryotes

“…Biofilms seem to be the most frequent lifestyle, with ca. 80% of bacterial and archaeal cells living in this form, which may serve as diversity incubators; planktonic lifestyle might be a secondary form. , Biofilms provide functions such as harvest and access to nutrients, shelter protection against environmental stresses, water retention to maintain extracellular enzyme activities, social cooperation, and horizontal gene transfer. , The occurrence of biofilm structures appears early in the fossil record (ca. 3.2 giga annum; Ga), a characteristic shared by prokaryote ‘living fossils’ present in hot springs and sea hydrothermal vents; bacteria and archaea lineages emerged at a similar time frame (ca.…”

Cyclic di‐GMP signaling—Where did you come from and where will you go?

“…Based on bioinformatics, cyclic di‐GMP is found in the deepest branching bacteria and, as predicted from the presence of genes encoding turnover proteins, also synthesized by archaea (Romling, 2023; Ryjenkov et al, 2005). Thus, cyclic di‐GMP, as its equally deeply branching analog cyclic di‐AMP (Braun et al, 2021; Römling, 2008; Witte et al, 2008), are ancient second messengers predicted to have been present in the proposed last universal common ancestor, LUCA, of bacteria and archaea.…”

“…Binding of cyclic di‐GMP to the elongation factor P facilitates translation of proline tracks in biofilm proteins and to the α‐L‐glutamate ligase RimK stimulates its enzymatic activity leading to C‐terminal glutaminylation of the ribosomal protein RpsF to modulate translation (Guo et al, 2022; Little et al, 2016). On the overall evolutionary time scale equally as the cyclic di‐GMP network encoded by genomes, cyclic di‐GMP binding sites of individual proteins can rapidly appear and disappear in evolution (Römling, 2023).…”