What are aquatic biofilms?
Aquatic environments are teeming with life, much of which exists unseen to the untrained eye. Beneath the water surface a hidden world thrives in which microbial communities play a pivotal role. Among these communities aquatic biofilms are the unsung heroes, silently shaping the health and integrity of whole ecosystems [1, 2].
Aquatic biofilms are ubiquitous three-dimensional communities of microorganisms comprised of a diverse array of bacteria, algae, and fungi, which adhere to submerged surfaces, such as rocks, sediments, or aquatic plants. The microorganisms are embedded in a slimy matrix of extracellular polymeric substances (EPS), creating a dynamic and multifaceted skin that blankets riverbeds, lake bottoms, and marine substrates.
The new term “microbial skin” was recently introduced to describe aquatic biofilms, highlighting their ecological and functional importance in aquatic ecosystems [1]. It emphasizes the role of the biofilms in shaping the physical, chemical, and biological characteristics of the surface of water bodies, much like how our skin functions as a barrier for our bodies.
A protective barrier
Just as our skin protects our bodies from external pathogens and helps regulate temperature, aquatic biofilms shield underlying sediments and organisms from external threats. One of their primary roles is serving as a physical barrier that can trap or restrict the diffusion of antibiotics, immune cells, pollutants, potential competitors, and invasive species, etc. [3, 4].
This protective capability is thanks mainly to the sticky EPS matrix which provides structural support, helping the biofilm adhere to surfaces and form stable three-dimensional structures. The EPS matrix is a complex mixture of various substances that are produced by biofilm-forming microorganisms. It primarily consists of polysaccharides (sugar-based molecules), but also contains proteins, DNA, and other organic molecules.
A stabilizing structure
Beyond protection, the EPS matrix also acts as a binding agent that effectively cements sediment and other particulate matter in place [5]. It reinforces the structural integrity of the benthic zone, such as riverbeds and lake bottoms, preventing erosion and sediment displacement caused by water flow and turbulence. Aquatic biofilms therefore contribute to the physical stability of aquatic habitats through their unique capacity to adhere to and consolidate substrates.
This stabilizing role is crucial for maintaining the physical structure of the habitat, which, in turn, supports a diverse range of aquatic organisms by providing stable niches and preventing the release of suspended particles that could disrupt the water column.
A host for diverse microorganisms
Like all natural microbiomes, such as those in the human gut or on our skin, aquatic biofilms foster a stunning array of microorganisms. They are composed of hundreds if not thousands of coexisting and interacting species of bacteria, archaea, algae, fungi, and sometimes protozoa, each contributing its unique genetic and metabolic capabilities [1].
The development of aquatic biofilms, and consequently their final microbial composition, is driven by environmental filtering. This includes water chemistry, temperature, substrate type and hydrodynamic conditions. The species succession dynamics and community assembly are strongly influenced by the initial species pool and any intra- and interspecific competition for resources.
How they form
Biofilm development begins with adhesion of planktonic bacteria to a submerged surface and production of EPS, which helps to anchor them to that substrate. Various bacterial strains belonging to the Sphingomonas family have been frequently identified as initiators of aquatic biofilm formation. They are thought to be well suited to this task due to their ability to rapidly produce exopolysaccharides with unique colloidal and gelling properties [6].
Depending on the colonization substrate and light conditions, other groups of microorganisms are also able to integrate the EPS matrix. For example, phototrophic microorganisms (diatoms, green algae, and cyanobacteria) contribute to the diversity of biofilms on rocks near the water surface, where light is available [7]. They form symbiotic relationships with the heterotrophic bacteria and are essential for primary production.
The highly diverse group of aquatic fungi, also known as hyphomycetes, dominate biofilms that colonize submerged wood or leaves [8]. They play a key role in decomposing recalcitrant organic matter so that it becomes more labile and can be easily assimilated by bacteria and higher trophic levels.
As biofilms mature the microbial community undergoes further diversification, with distinct layers of microorganisms developing within the biofilm structure. EPS production increases, providing structural support and protection to the biofilm. Nutrient gradients develop, creating microenvironments that support different microbial niches.
Finally, in established biofilms, a dynamic equilibrium is reached where microbial growth, detachment, and colonization processes are balanced. The biofilm continues to respond to environmental cues, such as changes in nutrient availability, flow conditions, and the presence of other organisms, maintaining its adaptability and functionality.
Advantages for resident microorganisms
Life in biofilms offers “strength in numbers” and represents a remarkable adaptation strategy by microorganisms. It allows them not only to endure challenging conditions but also to thrive and compete effectively in a variety of ecological niches.
Nutrient sharing and cycling
In addition to the physical protection conferred by the EPS matrix, biofilms retain and share out resources among their constituent microorganisms, better enabling them to survive when resources are scarce [3]. The extracellular matrix serves as a reservoir, storing essential nutrients and providing a consistent source of sustenance for the resident cells. By cooperatively using nutrients and metabolic byproducts, microorganisms within biofilms can outcompete free-living planktonic cells in resource-limited environments. This collaborative approach enhances the metabolic efficiency and growth of the microorganisms, enabling the biofilm to function as a coordinated and, to some extent, self-sufficient entity.
One key example is the symbiotic interactions between phototrophs and heterotrophs within biofilms, which involves the cycling of nutrients in a “microbial loop” [7]. Phototrophic microorganisms, such as algae and cyanobacteria, release organic matter into the environment through processes such as photosynthesis. Concurrently, heterotrophic bacteria decompose this organic matter, releasing essential nutrients such as nitrogen and phosphorus. These nutrients are in a form that can be readily absorbed and utilized by the phototrophic microorganisms for their growth and photosynthetic activities.
Genetic diversity
Microorganisms within biofilms also exhibit increased genetic diversity due to the proximity of numerous species and the resulting potential for horizontal gene transfer. This diversity enables biofilm communities to adapt rapidly to changing environmental conditions, as well as to develop resistance mechanisms against antimicrobial agents. Genetic diversity and adaptive potential are critical for the long-term survival of microorganisms, making biofilms an ideal strategy for thriving in dynamic ecosystems. This has far-reaching ecological implications.
Also key to the survival of aquatic biofilms is the high level of functional redundancy they harbor, in which diverse microorganisms perform analogous roles [9]. This redundancy provides a safety net to ensure that the biofilm can function effectively, as different species can compensate for each other’s functions. For instance, many different bacterial species within the biofilm can engage in the degradation of organic matter, nutrient cycling, and the production of EPS. Therefore, if one specific bacterial group is negatively affected by environmental changes or disturbances, other functionally similar bacteria can compensate, ensuring the continuity of vital biofilm functions.
How the “microbial skin” might interact with human skin
Research on how aquatic biofilms might interact with our own skin is scarce. However, evidence suggests that it is likely to be a multifaceted interaction that involves complex microbial dynamics and potential consequences for skin health.
The microorganisms
When individuals engage in activities involving natural water bodies, they may come into contact with aquatic biofilms, leading to the transfer of constituent microorganisms onto their skin. Depending on factors such as the specific microorganisms involved, the composition of the biofilm, and the overall health of their skin, this transfer might influence the delicate balance of the human skin microbiome.
While many of the microorganisms within biofilms are harmless or even beneficial, the transfer of pathogenic bacteria, such as specific strains of Bacillus spp. or Vibrio spp., from aquatic biofilms could contribute to skin infections. For instance, skin colonization by Staphylococcus aureus, a bacterium commonly found in aquatic biofilms, has been shown to exacerbate inflammation and sensitization of patients with atopic eczema [10, 11]. This notwithstanding, it is important to note that the presence of S. aureus in aquatic biofilms does not necessarily imply a direct threat to human health. It is essential to consider the specific strains and conditions involved.
The extracellular polymeric substances (EPS)
The EPS produced by biofilms may also contain a variety of compounds that could have implications for skin health. The impact of EPS on our skin is a nuanced and dynamic area of study, influenced by the diverse composition of these substances within microbial biofilms.
Polysaccharides, which constitute a significant proportion of EPS, contribute to the biofilm matrix and may influence skin hydration and barrier function. Proteins found in EPS have the potential to affect our skin proteins by participating in enzymatic reactions relevant to skin health. Nucleic acids, including DNA and RNA, contribute to biofilm stability and may have immunomodulatory effects on our skin. Lipids, encompassing various fatty acids and lipid molecules within EPS, can impact the skin’s lipid barrier, crucial for hydration and protection. Finally, any bioactive molecules present in EPS, such as signaling compounds or secondary metabolites, have the potential to interact with our skin cells, potentially modulating various physiological processes.
The specific impact of EPS on human skin health is contingent upon the microbial community, EPS concentration, duration of contact, and the intricate interplay with the skin’s natural defense mechanisms. While some components of EPS may contribute positively to skin well-being, others may pose challenges.
This emphasizes the need for further research to comprehend the multifaceted relationship between microbial biofilms, EPS, and skin health. Future research should explore these interactions to elucidate the implications for skin health and to develop strategies for promoting skin well-being in the context of environmental exposure. In the meantime, proper hygiene practices, such as thorough cleaning after water-related activities, can help minimize potential risks associated with exposure to aquatic biofilms.
References
- T.J. Battin, K. Besemer, M.M. Bengtsson, A.M. Romani, A.I. Packmann, The ecology and biogeochemistry of stream biofilms, Nature Reviews Microbiology, 14 (2016) 251-263.
- T.J. Battin, L.A. Kaplan, J.D. Newbold, C.M.E. Hansen, Contributions of microbial biofilms to ecosystem processes in stream mesocosms, Nature, 426 (2003) 439-442.
- H.-C. Flemming, J. Wingender, The biofilm matrix, Nature Reviews Microbiology, 8 (2010) 623-633.
- M. Burmolle, J.S. Webb, D. Rao, L.H. Hansen, S.J. Sorensen, S. Kjelleberg, Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms, Appl Environ Microbiol, 72 (2006) 3916-3923.
- E. Vignaga, D.M. Sloan, X. Luo, H. Haynes, V.R. Phoenix, W.T. Sloan, Erosion of biofilm-bound fluvial sediments, Nature Geoscience, 6 (2013) 770-774.
- L. Di Gregorio, V. Tandoi, R. Congestri, S. Rossetti, F. Di Pippo, Unravelling the core microbiome of biofilms in cooling tower systems, Biofouling, 33 (2017) 793-806.
- A. Bharti, K. Velmourougane, R. Prasanna, Phototrophic biofilms: diversity, ecology and applications, Journal of Applied Phycology, 29 (2017) 2729-2744.
- M.O. Gessner, C.M. Swan, C.K. Dang, B.G. McKie, R.D. Bardgett, D.H. Wall, S. Hättenschwiler, Diversity meets decomposition, Trends in Ecology & Evolution, 25 (2010) 372-380.
- A. Dopheide, G. Lear, Z. He, J. Zhou, G.D. Lewis, Functional Gene Composition, Diversity and Redundancy in Microbial Stream Biofilm Communities, PLOS ONE, 10 (2015) e0123179.
- M. Brandwein, D. Steinberg, S. Meshner, Microbial biofilms and the human skin microbiome, npj Biofilms and Microbiomes, 2 (2016) 3.
- V. Silva, M. Caniça, J.L. Capelo, G. Igrejas, P. Poeta, Diversity and genetic lineages of environmental staphylococci: a surface water overview, FEMS Microbiology Ecology, 96 (2020).
