Intertidal biofilm

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Biofilms in marine environments Various biofilm components (including bacteria, algae, and fungi) are embedded in a matrix of extracellular polymeric substances. Biofilm components in streams.jpg
Biofilms in marine environments Various biofilm components (including bacteria, algae, and fungi) are embedded in a matrix of extracellular polymeric substances.

An intertidal bioflim is a biofilm that forms on the intertidal region of bodies of water. Bacteria and various microorganisms, including algae and fungi, form communities of adhered cells called biofilms. [1] A matrix of extracellular polymeric substances (EPS) within the biofilm forms sticky coatings on individual sediment particles and detrital surfaces. [2] This feature protects bacteria against environmental stresses like temperature and pH fluctuations, UV exposure, changes in salinity, depletion of nutrients, antimicrobial agents, desiccation, and predation. [1] [2] Particularly, in the ever-changing environments of intertidal systems, biofilms can facilitate a range of microbial processes and create protective microenvironments where cells communicate with each other and regulate further biofilm formation via Quorum Sensing (QS). [2] , [3] While biofilm formation is advantageous to bacteria and other microorganisms involved, the attachment of microorganisms to ship hulls can increase fuel consumption and emission of greenhouse gases, as well as introduce Non-Indigenous Species (NIS), potentially resulting in harmful economic and ecological impacts on the receiving ecosystems. [4]

Contents

Stages of biofilm development 1) Initial Attachment 2) Irreversible Attachment 3) Maturation I 4) Maturation II 5) Dispersion. Biofilm id.JPG
Stages of biofilm development 1) Initial Attachment 2) Irreversible Attachment 3) Maturation I 4) Maturation II 5) Dispersion.

Formation and development

Biofilm formation

Biofilm formation begins with the initial attachment of microorganisms to a substrate, such as rocks, shells, or sand in the intertidal zone. This process occurs during the reversible attachment phase, in which the microorganisms only lightly adhere to the substrate. [5] In this phase, the bacteria are encompassed in small amounts of EPS; they are still capable of individual movement and may return to planktonic life. [5] , [6] Microorganisms may attach to the surface of substrates by weak Van der Waals forces and hydrophobic effects. [7] A study of Pseudomonas aeruginosa mutants showed that twitching motility by type IV pili contributes to the organism’s ability to aggregate on substrates. [8] Another mechanism by which bacteria may adhere to surfaces is the binary division of attached cells. [5]  Similar to colony formation on agar plates, as cells divide, the daughter cells spread expansively, forming cell clusters. [5] In all cases, adhesion depends on the microorganisms involved, the nature of the substrate, and the chemical and biological conditions of the environment.

The next stage is the irreversible attachment stage, in which microbes start producing EPS. This process creates a three-dimensional polymer network that acts as the biofilm matrix and encloses the bacteria. [9]  In this stage, EPS prevent bacterial cells from moving, keeping them in long-term close contact and allowing interactions such as cell-to-cell communication and horizontal gene transfer to occur. [9] In most biofilms, the microbes constitute less than 10% of the dry mass, while the EPS matrix can comprise over 90%. [9]

Biofilm development

Maturation

Following the irreversible phase, the next phase of the biofilm life cycle is maturation. In this stage, EPS play a critical role in protecting the biofilm from environmental fluctuations such as oxidative damage, antimicrobials, and host immune system response. [10]   Microcolonies are formed as a result of the aggregation of microbial cells and the increase of microbes with accessible nutrients. [6]   With the increase in cells, the biofilm matures and develops into a “tower” or “mushroom” like structure with a complex architecture of fluid-filled channels and pores. [5] , [6] , [10]

Detachment

Detachment, also known as dispersal, is the final stage of the biofilm life cycle. In this stage, cells are released from the biofilm matrix, individually or in clusters, and either resume planktonic life or attach to another surface. [5] , [6] Various factors can lead to cell detachment, including insufficient nutrients, competition, lack of oxygen, and environmental factors. [10]

Features

Taxonomic diversity

Marine biofilm communities have rich and diverse taxa, [11] with Cyanobacteria and Proteobacteria being the dominant phyla. [12] Actinobacteria , Bacteroidetes, and Planctomycetes are also considered to be dominant phyla but their relative abundances differ between locations. [12] Site-specific differences also arise within intertidal biofilms. For instance, intertidal biofilms in Río de la Plata contained high amounts of Betaproteobacteria from the Thauera genus, [13] whereas intertidal biofilms along the Pearl River Estuary contained Alphaproteobacteria and Gammaproteobacteria as the most prominent taxa. [14]

Extracellular Polymeric Substances (EPS)

Scanning electron micrograph of mixed-culture biofilm, showing the arrangement of bacterial cells and extracellular polymeric substances Mixed-culture biofilm.jpg
Scanning electron micrograph of mixed-culture biofilm, showing the arrangement of bacterial cells and extracellular polymeric substances

Diatoms are a major component of intertidal biofilms, [15] and they excrete EPS that support many functions, such as desiccation resistance, motility, and metabolite exchange. [16] The EPS produced by microalgae also enhance biofilm growth and help other members of the biofilm with adhesion and migration. [17] EPS are mostly composed of polysaccharides, but may also include proteins, nucleic acids, lipids, and low-molecular-weight, non-carbohydrate compounds. [16]

Seasonal variation

Intertidal biofilms exhibit stratification, where different microorganisms arrange themselves in layers based on factors like seasonality. Microalgae are found on the lower shore [18] but their distribution can change. During the winter, a greater abundance and biomass of microalgae are found on the upper shore compared to the lower shore. [19] Seasonal variability is also observed in the relative abundance of microalgae in intertidal biofilms. Specifically, microalgae in tropical and temperate intertidal biofilms are most abundant during winter and spring, with abundance decreasing in the warmer months. [20] Cyanobacteria are relatively less affected by seasonal variation. [21] This may be attributed to their greater tolerance to stressors such as temperature and insolation. [22]

Interactions within the biofilm

Interactions within biofilms are bidirectional. They can be affected by negative and positive feedback loops, as well as indirect effects. [23] These interactions contribute to the resilience and adaptability of intertidal biofilms. [24]

Trophic interactions

Within intertidal biofilms, trophic interactions exist between microphytobenthos and bacteria. [25] EPS, which are produced by microphytobenthos, act as a trophic resource, but their large size makes them difficult to break down and assimilate. [26] Bacteria secrete various enzymes like β-glucosidase to break down complex carbohydrate compounds in EPS. [27] These carbohydrates serve as a nutrient source for heterotrophic bacteria and sulfate-reducing bacteria (SRB), [2] as well as a carbon source for consumers such as marine invertebrates. [28]

Quorum Sensing (QS)

Biofilm communities facilitate both intra-species communication and inter-species communication through QS, which relies on the production and release of signaling molecules known as autoinducers. [29] When autoinducers reach a specific threshold concentration, signaling pathways are activated, resulting in physiological changes. [2] QS, alongside other methods of cell signaling regulation, is important for intertidal biofilms, as it allows them to survive in fluctuating environments and varying conditions. [30] This is because the expression of many genes in biofilms is shown to be density-dependent, with QS playing a crucial role in modulating feedback loops. [31] Autoinducer signals have also resulted in biofilms having a very different architecture compared to those with no QS capabilities. [32]

Various types of interactions within the biofilm(1) Communication through quorum sensing (2) Adaptations to varying conditions such as light Mature biofilm structure.png
Various types of interactions within the biofilm(1) Communication through quorum sensing (2) Adaptations to varying conditions such as light

Adaptations to varying conditions

Intertidal biofilms exhibit diverse adaptation mechanisms to cope with fluctuating conditions such as light stress, metal ion and oxidative stress, and desiccation stress.

Light stress

As intertidal biofilms are found in locations with fluctuating environmental conditions, biofilm microalgae are often damaged by the accumulation of reactive oxygen species (ROS). [33] High levels of ROS induce photoinhibition, inactivating the photosystem II protein D1 and negatively affecting primary productivity. [34] In these conditions, estuarine diatoms improve the efficiency of the xanthophyll cycle, [35] limiting the amount of photodamage and providing the biofilm with a photo-protective mechanism. [36] Vertical migration also allows members of the biofilm community to adapt to light stress. [37] Cells migrate toward the sediment surface when a tide leaves, then migrate downwards upon the arrival of an incoming tide. [38]

Metal ion and oxidative stress

Industrial activities in intertidal regions lead to increased concentrations of heavy metals such as copper, zinc, and cadmium, resulting in metal ion stress for the biofilms. [2] To adapt to these conditions, genes involved in metal ion transport and secondary metabolism are over-expressed by intertidal microorganisms, allowing them to transport the heavy metals against electrochemical gradients and prevent toxicity. [39] The expression of EPS is also enhanced when exposed to increased levels of heavy metals. [39] EPS serves as an adaptive mechanism to tolerate metal ion stress as its components have functional groups that bind toxic heavy metals and prevent heavy metal toxicity. [40]

Desiccation stress

Desiccation leads to a significant decrease in the photosynthetic activity of microphytobenthos in biofilms. [41] To slow down desiccation, diatoms and bacteria in the biofilm produce EPS, decreasing the rate of water loss and dehydration. [42] EPS produced from a Microbacterium species have also been identified to have surfactant properties, playing a role in protecting against desiccation. [43] Alternatively, another protection mechanism against desiccation involves vertical migration, the same strategy that microorganisms use to protect against light stress. Motile diatoms migrate downwards when exposed to extreme light and temperature conditions, [44] as this allows them to be present in a moist microenvironment and mitigate the effects on photosynthetic activity.

Nutrient cycling in the marine environment Nutrient-cycle hg.png
Nutrient cycling in the marine environment

Ecological impact and functions

The cohesive nature of EPS contributes not only to the sediment's stability, preventing its resuspension under erosion, but also enhances flocculation processes. Flocculation processes involve the accumulation of fine sediments into larger flocs, modifying biogeochemical exchanges. This stabilization is important for geomorphologic evolution and the ecosystem health of coastal areas. [45] A study from Jiangsu coast, China concluded that flocculation processes affect the density, particle size, and settling velocity of suspended particles, which are essential for sedimentation and sediment transport. [45] These processes are also important in biogeochemical cycles for nutrients and heavy metals due to the adsorption ability and transport function of particles in flocs. [45]

Intertidal marine biofilms on rocky substrates significantly impact estuarine carbon and nutrient dynamics. Biofilms in the Douro River estuary were observed to engage actively in biogeochemical processes, showing considerable net primary production that greatly exceeded respiration rates. [46] These biofilms play a key role in nutrient fluxes, consistently removing nitrate and silicate from the water column while exhibiting variable fluxes of ammonium depending on light conditions, indicating a preference for ammonium assimilation by primary producers within the biofilms. Despite their limited spatial coverage, rocky biofilms account for a significant portion of the nitrate and silicate uptake compared to adjacent sandy and muddy sediments within the estuary. [46]

Impacts of anthropogenic activities

Biofouling on marine structures

The attachment and growth of marine organisms on submerged artificial structures, such as ship hulls and aquaculture infrastructures, can cause ecological and economic issues. This biofouling leads to increased drag resistance, fuel consumption, and greenhouse gas emissions for ships. It also restricts water exchange, raises disease risk, and causes deformation in aquaculture setups. [4]

Introduction of Non-Indigenous Species (NIS)

Biofouling on ships, both as hull fouling and through solid ballast (sand, rocks, and soil), is a major pathway for the arrival of NIS into new regions. [4] This introduces significant risks to receiving ecosystems, potentially resulting in significant economic and ecological impacts. Ports, which are primary receivers of maritime trade goods, are particularly at high risk for NIS introductions. [4] Monitoring NIS presence and impacts, while implementing preventive measures to minimize their settlement, are critical for marine environmental management.

Resilience of biofilms on human activities

A research study conducted along the southeast coast of Brazil showed that human activities, such as trampling, were minimal. A trend of increased variability in biofilm biomass was observed with more intense trampling but no significant differences were found across trampling frequencies and intensities. The microorganisms' small size, which prevents complete removal by trampling, and the biofilms' capacity for rapid recovery may contribute to their high resilience to physical disturbance. [47]

Related Research Articles

<span class="mw-page-title-main">Biofilm</span> Aggregation of bacteria or cells on a surface

A biofilm is a syntrophic community of microorganisms in which cells stick to each other and often also to a surface. These adherent cells become embedded within a slimy extracellular matrix that is composed of extracellular polymeric substances (EPSs). The cells within the biofilm produce the EPS components, which are typically a polymeric combination of extracellular polysaccharides, proteins, lipids and DNA. Because they have a three-dimensional structure and represent a community lifestyle for microorganisms, they have been metaphorically described as "cities for microbes".

<span class="mw-page-title-main">Seagrass</span> Plants that grow in marine environments

Seagrasses are the only flowering plants which grow in marine environments. There are about 60 species of fully marine seagrasses which belong to four families, all in the order Alismatales. Seagrasses evolved from terrestrial plants which recolonised the ocean 70 to 100 million years ago.

The purple sulfur bacteria (PSB) are part of a group of Pseudomonadota capable of photosynthesis, collectively referred to as purple bacteria. They are anaerobic or microaerophilic, and are often found in stratified water environments including hot springs, stagnant water bodies, as well as microbial mats in intertidal zones. Unlike plants, algae, and cyanobacteria, purple sulfur bacteria do not use water as their reducing agent, and therefore do not produce oxygen. Instead, they can use sulfur in the form of sulfide, or thiosulfate (as well, some species can use H2, Fe2+, or NO2−) as the electron donor in their photosynthetic pathways. The sulfur is oxidized to produce granules of elemental sulfur. This, in turn, may be oxidized to form sulfuric acid.

Microbial intelligence is the intelligence shown by microorganisms. The concept encompasses complex adaptive behavior shown by single cells, and altruistic or cooperative behavior in populations of like or unlike cells mediated by chemical signalling that induces physiological or behavioral changes in cells and influences colony structures.

<span class="mw-page-title-main">Flavobacteriia</span> Class of bacteria

The class Flavobacteriia is composed of a single class of environmental bacteria. It contains the family Flavobacteriaceae, which is the largest family in the phylum Bacteroidota. This class is widely distributed in soil, fresh, and seawater habitats. The name is often spelt Flavobacteria, but was officially named Flavobacteriia in 2012.

<span class="mw-page-title-main">Extracellular polymeric substance</span> Gluey polymers secreted by microorganisms to form biofilms

Extracellular polymeric substances (EPSs) are natural polymers of high molecular weight secreted by microorganisms into their environment. EPSs establish the functional and structural integrity of biofilms, and are considered the fundamental component that determines the physicochemical properties of a biofilm. EPS in the matrix of biofilms provides compositional support and protection of microbial communities from the harsh environments. Components of EPS can be of different classes of polysaccharides, lipids, nucleic acids, proteins, lipopolysaccharides, and minerals. This chemical formula is (C135H217N15Na2O74P10).

<span class="mw-page-title-main">Phototrophic biofilm</span> Microbial communities including microorganisms which use light as their energy source

Phototrophic biofilms are microbial communities generally comprising both phototrophic microorganisms, which use light as their energy source, and chemoheterotrophs. Thick laminated multilayered phototrophic biofilms are usually referred to as microbial mats or phototrophic mats. These organisms, which can be prokaryotic or eukaryotic organisms like bacteria, cyanobacteria, fungi, and microalgae, make up diverse microbial communities that are affixed in a mucous matrix, or film. These biofilms occur on contact surfaces in a range of terrestrial and aquatic environments. The formation of biofilms is a complex process and is dependent upon the availability of light as well as the relationships between the microorganisms. Biofilms serve a variety of roles in aquatic, terrestrial, and extreme environments; these roles include functions which are both beneficial and detrimental to the environment. In addition to these natural roles, phototrophic biofilms have also been adapted for applications such as crop production and protection, bioremediation, and wastewater treatment.

<span class="mw-page-title-main">Microbial mat</span> Multi-layered sheet of microorganisms

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<span class="mw-page-title-main">Sea ice microbial communities</span> Groups of microorganisms living within and at the interfaces of sea ice

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<span class="mw-page-title-main">Viral shunt</span>

The viral shunt is a mechanism that prevents marine microbial particulate organic matter (POM) from migrating up trophic levels by recycling them into dissolved organic matter (DOM), which can be readily taken up by microorganisms. The DOM recycled by the viral shunt pathway is comparable to the amount generated by the other main sources of marine DOM.

<span class="mw-page-title-main">Marine primary production</span> Marine synthesis of organic compounds

Marine primary production is the chemical synthesis in the ocean of organic compounds from atmospheric or dissolved carbon dioxide. It principally occurs through the process of photosynthesis, which uses light as its source of energy, but it also occurs through chemosynthesis, which uses the oxidation or reduction of inorganic chemical compounds as its source of energy. Almost all life on Earth relies directly or indirectly on primary production. The organisms responsible for primary production are called primary producers or autotrophs.

<span class="mw-page-title-main">Marine protists</span> Protists that live in saltwater or brackish water

Marine protists are defined by their habitat as protists that live in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Life originated as marine single-celled prokaryotes and later evolved into more complex eukaryotes. Eukaryotes are the more developed life forms known as plants, animals, fungi and protists. Protists are the eukaryotes that cannot be classified as plants, fungi or animals. They are mostly single-celled and microscopic. The term protist came into use historically as a term of convenience for eukaryotes that cannot be strictly classified as plants, animals or fungi. They are not a part of modern cladistics because they are paraphyletic.

<span class="mw-page-title-main">Phytobenthos</span>

Phytobenthos (from Greek φυτόν and βένθος are autotrophic organisms found attached to bottom surfaces aquatic environments, such as rocks, sediments, or even other organisms. This photosynthetic community includes single-celled or filamentous cyanobacteria, microalgae, and macrophytes. Phytobenthos are highly diverse, and can be found in freshwater and marine environments, as well as transitional water systems. However, their distribution and availability still depend on the factors and stressors that exist in the environment. Because phytobenthos are autotrophs, they need to be able to subsist where it is still possible to perform photosynthesis. Similar to phytoplankton, phytobenthos contribute to the aquatic food web for grazers and heterotrophic bacteria, and researchers have also been studying their health as an indicator for water quality and environmental integrity of aquatic ecosystems.

<span class="mw-page-title-main">Parasites of phytoplankton</span>

Phytoplankton are characterized as organisms which are unable to swim against a current and produce their own organic carbon via photosynthesis. They are responsible for producing approximately 50 percent of the Earth’s primary productivity and are therefore crucial in maintaining both marine ecosystems and adding a significant amount of oxygen to the atmosphere. However, as with other organisms, phytoplankton are hosts to many diverse forms of parasites, including, but not limited to, fungal- and non-fungal zoosporic parasites, Dinoflagellates, Cercozoans, and viruses. Parasites use nutrients from their hosts, at that organisms expense, and display diverse methods of infection. Parasites can play integral roles in the dynamics and interactions between phytoplankton and their communities, such as controlling population abundance, distribution and biodiversity.

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