Intertidal biofilm

Redirect to:

* Intertidal biofilms

Biofilms in Marine Environments Various biofilm components (including bacteria, algae, and fungi) are embedded in a matrix of extracellular polymeric substances. |
This template is not to be used in article space.

This is the sandbox page where you will draft your initial Wikipedia contribution.

If you're starting a new article, you can develop it here until it's ready to go live.

If you're working on improvements to an existing article, copy only one section at a time of the article to this sandbox to work on, and be sure to use an edit summary linking to the article you copied from. Do not copy over the entire article. You can find additional instructions here.

Remember to save your work regularly using the "Publish page" button. (It just means 'save'; it will still be in the sandbox.) You can add bold formatting to your additions to differentiate them from existing content.

* Bibliography sandbox

|

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]

Five Stages of Biofilm Development 1) Initial Attachment 2) Irreversible Attachment 3) Maturation I 4) Maturation II 5) Dispersion.

### Formation and Development[edit]

#### Biofilm Formation[edit]

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[edit]

##### Maturation[edit]

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] During this phase, microcolonies are formed as a result of the aggregation of microbial cells and from the increase of microbes with accessible nutrients.[6] With the increase of 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[edit]

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[edit]

#### Taxonomic Diversity[edit]

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

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] These EPSs are mostly composed of polysaccharides, but may also include proteins, nucleic acids, lipids, and low-molecular-weight, non-carbohydrate compounds.[16]

#### Seasonal Variation[edit]

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 changes. 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 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[edit]

Interactions within biofilms are more complex compared to those in vitro. Unlike bacteria in culture, interactions within the biofilm are bidirectional and are 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[edit]

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)[edit]

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 in comparison 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

### Adaptations to Varying Conditions[edit]

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[edit]

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] Another mechanism by which members of the biofilm community are able to adapt to light stress involves vertical migration.[37] Cells migrate toward the sediment surface when a tide leaves, followed by a downward migration upon an incoming tide.[38]

#### Metal Ion and Oxidative Stress[edit]

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[edit]

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, implicating its role in protection against desiccation.[43] Alternatively, another protection mechanism against desiccation involves vertical migration, the same strategy that microorganisms use to protect against light stress. Specifically, 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

### Ecological Impact and Functions[edit]

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, as highlighted by a study conducted in the Douro River estuary.[45] These biofilms were observed to engage actively in biogeochemical processes, showing considerable net primary production that greatly exceeded respiration rates. They 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, underscoring their importance in nutrient cycling within the estuary.[46]

### Impacts of Anthropogenic Activities[edit]

#### Biofouling on Marine Structures[edit]

The attachment and growth of marine organisms on submerged artificial structures, such as ship hulls and aquaculture infrastructures, are identified as 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)[edit]

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[edit]

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]

### References[edit]

1. ^ a b de Carvalho, Carla C. C. R. (2018). "Marine Biofilms: A Successful Microbial Strategy With Economic Implications". Frontiers in Marine Science. 5. doi:10.3389/fmars.2018.00126. ISSN 2296-7745.
2. ^ a b c d e f Decho, Alan W (2000-07-01). "Microbial biofilms in intertidal systems: an overview". Continental Shelf Research. 20 (10): 1257–1273. Bibcode:2000CSR....20.1257D. doi:10.1016/S0278-4343(00)00022-4. ISSN 0278-4343.
3. ^ Li, Yung-Hua; Tian, Xiaolin (2012-02-23). "Quorum Sensing and Bacterial Social Interactions in Biofilms". Sensors. 12 (3): 2519–2538. Bibcode:2012Senso..12.2519L. doi:10.3390/s120302519. ISSN 1424-8220. PMC 3376616. PMID 22736963.
4. ^ a b c d Cacabelos, Eva; Ramalhosa, Patrício; Canning-Clode, João; Troncoso, Jesús S.; Olabarria, Celia; Delgado, Cristina; Dobretsov, Sergey; Gestoso, Ignacio (2020-03-16). "The Role of Biofilms Developed under Different Anthropogenic Pressure on Recruitment of Macro-Invertebrates". International Journal of Molecular Sciences. 21 (6): 2030. doi:10.3390/ijms21062030. ISSN 1422-0067. PMC 7139543. PMID 32188145.
5. ^ a b c d e f Stoodley, P.; Sauer, K.; Davies, D. G.; Costerton, J. W. (2002-04-19). "Biofilms as Complex Differentiated Communities". Annual Review of Microbiology. 56 (1): 187–209. doi:10.1146/annurev.micro.56.012302.160705. ISSN 0066-4227. PMID 12142477.
6. ^ a b c d De Silva, L. A. D. S.; Heo, Gang-Joon (2022-12-24). "Biofilm formation of pathogenic bacteria isolated from aquatic animals". Archives of Microbiology. 205 (1): 36. doi:10.1007/s00203-022-03332-8. ISSN 1432-072X. PMID 36565346.
7. ^ Briandet, R; Herry, J. -M; Bellon-Fontaine, M. -N (2001-08-01). "Determination of the van der Waals, electron donor and electron acceptor surface tension components of static Gram-positive microbial biofilms". Colloids and Surfaces B: Biointerfaces. 21 (4): 299–310. doi:10.1016/S0927-7765(00)00213-7. ISSN 0927-7765. PMID 11397632.
8. ^ O'Toole, George A.; Kolter, Roberto (2002-03-01). "Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development". Molecular Microbiology. 30 (2): 295–304. doi:10.1046/j.1365-2958.1998.01062.x. ISSN 0950-382X. PMID 9791175.
9. ^ a b c Flemming, Hans-Curt; Wingender, Jost (2010-09-02). "The biofilm matrix". Nature Reviews Microbiology. 8 (9): 623–633. doi:10.1038/nrmicro2415. ISSN 1740-1534.
10. ^ a b c Rather, Muzamil Ahmad; Gupta, Kuldeep; Mandal, Manabendra (2021-09-23). "Microbial biofilm: formation, architecture, antibiotic resistance, and control strategies". Brazilian Journal of Microbiology. 52 (4): 1701–1718. doi:10.1007/s42770-021-00624-x. ISSN 1517-8382. PMC 8578483. PMID 34558029.
11. ^ Wang, Shougang; Su, Xiaoyan; Cui, Han; Wang, Meng; Hu, Xiaoli; Ding, Wei; Zhang, Weipeng (2022-06-12). "Microbial Richness of Marine Biofilms Revealed by Sequencing Full-Length 16S rRNA Genes". Genes. 13 (6): 1050. doi:10.3390/genes13061050. ISSN 2073-4425. PMC 9223118. PMID 35741812.
12. ^ a b Lee, On On; Chung, Hong Chun; Yang, Jiangke; Wang, Yong; Dash, Swagatika; Wang, Hao; Qian, Pei-Yuan (2014-07-09). "Molecular techniques revealed highly diverse microbial communities in natural marine biofilms on polystyrene dishes for invertebrate larval settlement". Microbial Ecology. 68 (1): 81–93. Bibcode:2014MicEc..68...81L. doi:10.1007/s00248-013-0348-3. ISSN 1432-184X. PMID 24402362.
13. ^ Piccini, C.; García-Alonso, J. (2015-02-28). "Bacterial diversity patterns of the intertidal biofilm in urban beaches of Río de la Plata". Marine Pollution Bulletin. Marine pollution and assessment of marine status in Latin America. 91 (2): 476–482. Bibcode:2015MarPB..91..476P. doi:10.1016/j.marpolbul.2014.08.039. ISSN 0025-326X.
14. ^ Mai, Y. Z.; Peng, S. Y.; Lai, Z. N. (2020-01-01). "Structural and functional diversity of biofilm bacterial communities along the Pearl River Estuary, South China". Regional Studies in Marine Science. 33: 100926. Bibcode:2020RSMS...3300926M. doi:10.1016/j.rsma.2019.100926. ISSN 2352-4855.
15. ^ Smith, David J.; Underwood, Graham J. C. (2003-12-22). "Exopolymer production by intertidal epipelic diatoms". Limnology and Oceanography. 43 (7): 1578–1591. doi:10.4319/lo.1998.43.7.1578. ISSN 0024-3590.
16. ^ a b Underwood, Graham J. C.; Paterson, David M. (2003-01-01), "The importance of extracellular carbohydrate productionby marine epipelic diatoms", Advances in Botanical Research, vol. 40, Academic Press, pp. 183–240, retrieved 2024-04-04
17. ^ Lundkvist, M.; Gangelhof, U.; Lunding, J.; Flindt, M. R. (2007-11-01). "Production and fate of extracellular polymeric substances produced by benthic diatoms and bacteria: A laboratory study". Estuarine, Coastal and Shelf Science. Hydrodynamic control of aquatic ecosystem processes. 75 (3): 337–346. Bibcode:2007ECSS...75..337L. doi:10.1016/j.ecss.2007.04.034. ISSN 0272-7714.
18. ^ Aleem, A (1950). "Distribution and Ecology of British Marine Littoral Diatoms". British Ecology Society. 38 (1): 75–106. Bibcode:1950JEcol..38...75A. doi:10.2307/2256526. JSTOR 2256526 - via JSTOR.
19. ^ Thompson, R. C.; Norton, T. A.; Hawkins, S. J. (2004). "Physical Stress and Biological Control Regulate the Producer-Consumer Balance in Intertidal Biofilms". Ecology. 85 (5): 1372–1382. Bibcode:2004Ecol...85.1372T. doi:10.1890/03-0279. ISSN 0012-9658. JSTOR 3450178.
20. ^ Hill, A. S.; Hawkins, S. J. (2009-05-11). "Seasonal And Spatial Variation of Epilithic Micro Algal Distribution and Abundance and its Ingestion By Patella Vulgata on A Moderately Exposed Rocky Shore". Journal of the Marine Biological Association of the United Kingdom. 71 (2): 403–423. doi:10.1017/S0025315400051675. ISSN 1469-7769.
21. ^ Mak, Y. M; Williams, Gray A (1999-01-31). "Littorinids control high intertidal biofilm abundance on tropical, Hong Kong rocky shores". Journal of Experimental Marine Biology and Ecology. 233 (1): 81–94. doi:10.1016/S0022-0981(98)00122-1. ISSN 0022-0981.
22. ^ Yadav, Priya; Singh, Rahul Prasad; Rana, Shashank; Joshi, Diksha; Kumar, Dharmendra; Bhardwaj, Nikunj; Gupta, Rajan Kumar; Kumar, Ajay (2022-12-09). "Mechanisms of Stress Tolerance in Cyanobacteria under Extreme Conditions". Stresses. 2 (4): 531–549. doi:10.3390/stresses2040036. ISSN 2673-7140.
23. ^ Worm, Boris; Duffy, J.Emmett (2003-12-01). "Biodiversity, productivity and stability in real food webs". Trends in Ecology & Evolution. 18 (12): 628–632. doi:10.1016/j.tree.2003.09.003. ISSN 0169-5347.
24. ^ Paine, R. T. (1969-01-15). "A Note on Trophic Complexity and Community Stability". The American Naturalist. 103 (929): 91–93. doi:10.1086/282586. ISSN 0003-0147.
25. ^ Hubas, Cédric; Passarelli, Claire; Paterson, David M. (2018), Beninger, Peter G. (ed.), "Microphytobenthic Biofilms: Composition and Interactions", Mudflat Ecology, Cham: Springer International Publishing, pp. 63–90, doi:10.1007/978-3-319-99194-8_4, ISBN 978-3-319-99194-8, retrieved 2024-04-04
26. ^ Hoppe, Hans-Georg (1983). "Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates". Marine Ecology Progress Series. 11 (3): 299–308. Bibcode:1983MEPS...11..299H. doi:10.3354/meps011299. ISSN 0171-8630. JSTOR 44634717.
27. ^ Mckew; Dumbrell; Taylor; McGenity; Underwood (2013-06-01). "Differences between aerobic and anaerobic degradation of microphytobenthic biofilm-derived organic matter within intertidal sediments". academic.oup.com. Retrieved 2024-04-04.
28. ^ Herman, Peter M. J.; Middelburg, Jack J.; Widdows, John; Lucas, Cathy H.; Heip, Carlo H. R. (2000-10-05). "Stable isotopes as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos". Marine Ecology Progress Series. 204: 79–92. Bibcode:2000MEPS..204...79H. doi:10.3354/meps204079. ISSN 0171-8630.
29. ^ Bassler, Bonnie L.; Losick, Richard (2006-04-21). "Bacterially Speaking". Cell. 125 (2): 237–246. doi:10.1016/j.cell.2006.04.001. ISSN 0092-8674.
30. ^ Montgomery, Kate; Charlesworth, James C.; LeBard, Rebecca; Visscher, Pieter T.; Burns, Brendan P. (2013-01-29). "Quorum Sensing in Extreme Environments". Life : Open Access Journal. 3 (1): 131–148. Bibcode:2013Life....3..131M. doi:10.3390/life3010131. ISSN 2075-1729. PMC 4187201. PMID 25371335.
31. ^ Waters, Christopher M.; Bassler, Bonnie L. (2005-11-01). "QUORUM SENSING: Cell-to-Cell Communication in Bacteria". Annual Review of Cell and Developmental Biology. 21 (1): 319–346. doi:10.1146/annurev.cellbio.21.012704.131001. ISSN 1081-0706. PMID 16212498.
32. ^ Davies, D. G.; Parsek, M. R.; Pearson, J. P.; Iglewski, B. H.; Costerton, J. W.; Greenberg, E. P. (1998-04-10). "The involvement of cell-to-cell signals in the development of a bacterial biofilm". Science (New York, N.Y.). 280 (5361): 295–298. Bibcode:1998Sci...280..295D. doi:10.1126/science.280.5361.295. ISSN 0036-8075. PMID 9535661.
33. ^ Roncarati, F.; Rijstenbil, J. W.; Pistocchi, R. (2008-02-01). "Photosynthetic performance, oxidative damage and antioxidants in Cylindrotheca closterium in response to high irradiance, UVB radiation and salinity". Marine Biology. 153 (5): 965–973. Bibcode:2008MarBi.153..965R. doi:10.1007/s00227-007-0868-9. ISSN 1432-1793.
34. ^ Nishiyama, Yoshitaka; Allakhverdiev, Suleyman I.; Murata, Norio (2006-07-01). "A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II". Biochimica et Biophysica Acta (BBA) - Bioenergetics. 1757 (7): 742–749. doi:10.1016/j.bbabio.2006.05.013. ISSN 0005-2728.
35. ^ Serôdio, J.; Cruz, S.; Vieira, S.; Brotas, V. (2005-12-13). "Non-photochemical quenching of chlorophyll fluorescence and operation of the xanthophyll cycle in estuarine microphytobenthos". Journal of Experimental Marine Biology and Ecology. 326 (2): 157–169. doi:10.1016/j.jembe.2005.05.011. ISSN 0022-0981.
36. ^ Lavaud, Johann; Strzepek, Robert F.; Kroth, Peter G. (2007-05-17). "Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate". Limnology and Oceanography. 52 (3): 1188–1194. Bibcode:2007LimOc..52.1188L. doi:10.4319/lo.2007.52.3.1188. ISSN 0024-3590.
37. ^ Van Colen, Carl; Underwood, Graham J. C.; Serôdio, João; Paterson, David M. (2014-09-01). "Ecology of intertidal microbial biofilms: Mechanisms, patterns and future research needs". Journal of Sea Research. Trophic significance of microbial biofilm in tidal flats. 92: 2–5. Bibcode:2014JSR....92....2V. doi:10.1016/j.seares.2014.07.003. ISSN 1385-1101.
38. ^ Consalvey, Mireille; Paterson, David M.; Underwood, Graham J. C. (2004-11-02). "The Ups and Downs of Life in a Benthic Biofilm: Migration of Benthic Diatoms". Diatom Research. 19 (2): 181–202. Bibcode:2004DiaRe..19..181C. doi:10.1080/0269249X.2004.9705870. ISSN 0269-249X.
39. ^ a b Beech, I. B.; Cheung, C. W. S. (1995-01-01). "Interactions of exopolymers produced by sulphate-reducing bacteria with metal ions". International Biodeterioration & Biodegradation. Biosorption and Bioremediation. 35 (1): 59–72. doi:10.1016/0964-8305(95)00082-G. ISSN 0964-8305.
40. ^ Braissant, O.; Decho, A. W.; Dupraz, C.; Glunk, C.; Przekop, K. M.; Visscher, P. T. (2007-09-06). "Exopolymeric substances of sulfate-reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals". Geobiology. 5 (4): 401–411. Bibcode:2007Gbio....5..401B. doi:10.1111/j.1472-4669.2007.00117.x. ISSN 1472-4677.
41. ^ Coelho, H.; Vieira, S.; Serôdio, J. (2009-12-15). "Effects of desiccation on the photosynthetic activity of intertidal microphytobenthos biofilms as studied by optical methods". Journal of Experimental Marine Biology and Ecology. 381 (2): 98–104. doi:10.1016/j.jembe.2009.09.013. ISSN 0022-0981.
42. ^ Roberson, Emily B.; Firestone, Mary K. (1992-04-01). "Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp". Applied and Environmental Microbiology. 58 (4): 1284–1291. Bibcode:1992ApEnM..58.1284R. doi:10.1128/aem.58.4.1284-1291.1992. ISSN 0099-2240. PMC 195588. PMID 16348695.
43. ^ Ortega-Morales, B. O.; Santiago-García, J. L.; Chan-Bacab, M. J.; Moppert, X.; Miranda-Tello, E.; Fardeau, M. L.; Carrero, J. C.; Bartolo-Pérez, P.; Valadéz-González, A.; Guezennec, J. (2007-01-01). "Characterization of extracellular polymers synthesized by tropical intertidal biofilm bacteria". Journal of Applied Microbiology. 102 (1): 254–264. doi:10.1111/j.1365-2672.2006.03085.x. ISSN 1364-5072. PMID 17184342.
44. ^ Serôdio, João; Coelho, Helena; Vieira, Sónia; Cruz, Sónia (2006-07-01). "Microphytobenthos vertical migratory photoresponse as characterised by light-response curves of surface biomass". Estuarine, Coastal and Shelf Science. Ecological and Management Implications on Seagrass Landscapes. 68 (3): 547–556. Bibcode:2006ECSS...68..547S. doi:10.1016/j.ecss.2006.03.005. ISSN 0272-7714.
45. ^ a b c d Li, Jiasheng; Chen, Xindi; Townend, Ian; Shi, Benwei; Du, Jiabi; Gao, Jianhua; Chuai, Xiaowei; Gong, Zheng; Wang, Ya Ping (2021-04-01). "A comparison study on the sediment flocculation process between a bare tidal flat and a clam aquaculture mudflat: The important role of sediment concentration and biological processes". Marine Geology. 434: 106443. Bibcode:2021MGeol.43406443L. doi:10.1016/j.margeo.2021.106443. ISSN 0025-3227.
46. ^ Bordalo, Adriano (2003-01-01). "Intertidal biofilms on rocky substratum can play a major role in estuarine carbon and nutrient dynamics". Marine Ecology Progress. 258: 275. Bibcode:2003MEPS..258..275M. doi:10.3354/meps258275.
47. ^ Leite, Lucas G.; Ciotti, Áurea M.; Christofoletti, Ronaldo A. (2012-08-01). "Abundance of biofilm on intertidal rocky shores: Can trampling by humans be a negative influence?". Marine Environmental Research. 79: 111–115. Bibcode:2012MarER..79..111L. doi:10.1016/j.marenvres.2012.06.001. ISSN 0141-1136.