Mechanisms of microbial co-aggregation in mixed anaerobic cultures

Abstract

Co-aggregation of anaerobic microorganisms into suspended microbial biofilms (aggregates) serves ecological and biotechnological functions. Tightly packed aggregates of metabolically interdependent bacteria and archaea play key roles in cycling of carbon and nitrogen. Additionally, in biotechnological applications, such as wastewater treatment, microbial aggregates provide a complete metabolic network to convert complex organic material. Currently, experimental data explaining the mechanisms behind microbial co-aggregation in anoxic environments is scarce and scattered across the literature. To what extent does this process resemble co-aggregation in aerobic environments? Does the limited availability of terminal electron acceptors drive mutualistic microbial relationships, contrary to the commensal relationships observed in oxygen-rich environments? And do co-aggregating bacteria and archaea, which depend on each other to harvest the bare minimum Gibbs energy from energy-poor substrates, use similar cellular mechanisms as those used by pathogenic bacteria that form biofilms? Here, we provide an overview of the current understanding of why and how mixed anaerobic microbial communities co-aggregate and discuss potential future scientific advancements that could improve the study of anaerobic suspended aggregates. KEY POINTS: • Metabolic dependency promotes aggregation of anaerobic bacteria and archaea • Flagella, pili, and adhesins play a role in the formation of anaerobic aggregates • Cyclic di-GMP/AMP signaling may trigger the polysaccharides production in anaerobes.

Keywords: Anaerobic biofilm; Cell-to-cell adhesion; Co-aggregation; Exopolysaccharides; Syntrophy.

Fig. 1

Examples of microbial aggregates in anoxic (upper pane) and oxic/microaerophilic environments (bottom pane). Images of anaerobic methane-oxidizing aggregates are confocal laser scanning micrographs depicting hybridization with the fluorescent probes for archaea (red or pink) and bacteria (green), while blue color depicts general DNA stain. Images of aggregates reproduced with permission (Knittel and Boetius ; Jagersma et al. ; Gonzalez-Gil and Holliger ; Laurenceau-Cornec et al. ; Wilbanks et al. ; Lin et al. ; Chajwa et al. 2023)

Fig. 2

Key microbial symbiotic relationships within A anaerobic granules from anaerobic digesters, B anaerobic methane oxidation aggregates, and C anaerobic ammonia oxidation aggregates. Illustration was created with BioRender.com

Fig. 3

A 4-step conceptual model of co-aggregation in mixed anaerobic cultures which proceeds through: (1) mutualistic metabolic interactions, (2) population growth and extracellular signaling, (3) “first contact” and loss of motility, (4) aggregate maturation by expansion of EPS matrixome. Detailed description of the steps can be found in the text above. Illustration created with BioRender.com