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Mukhi Et Al 2022 Beneficial Biofilms A Minireview of Strategies To Enhance Biofilm Formation For Biotechnological

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MINIREVIEW

Beneficial Biofilms: a Minireview of Strategies To Enhance


Biofilm Formation for Biotechnological Applications
Mayur Mukhi,a A. S. Vishwanathana

WATER Laboratory, Department of Biosciences, Sri Sathya Sai Institute of Higher Learning, Prasanthi Nilayam, Puttaparthi, Andhra Pradesh, India
a

ABSTRACT The capacity of bacteria to form biofilms is an important trait for their sur-
vival and persistence. Biofilms occur naturally in soil and aquatic environments, are asso-
ciated with animals ranging from insects to humans, and are also found in built environ-
ments. They are typically encountered as a challenge in health care, food industry, and
water supply ecosystems. In contrast, they are known to play a key role in the industrial
production of commercially valuable products, environmental remediation processes,
and microbe-catalyzed electrochemical systems for energy and resource recovery from
wastewater. While there are many recent articles on biofilm control and removal, review
articles on promoting biofilm growth for biotechnological applications are unavailable.
Biofilm formation is a tightly regulated response to perturbations in the external envi-
ronment. The multistage process, mediated by an assortment of proteins and signaling
systems, involves the attachment of bacterial cells to a surface followed by their aggre-
gation in a matrix of extracellular polymeric substances. Biofilms can be promoted by
altering the external environment in a controlled manner, supplying molecules that trig-
ger the aggregation of cells and engineering genes associated with biofilm develop-
ment. This minireview synthesizes findings from studies that have described such strat-
egies and highlights areas needing research attention.

KEYWORDS biofilm engineering, EPS matrix, biofilms, biotechnology, quorum sensing

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B acteria aggregate to form biofilms as a stress response mechanism when subjected to
unfavorable temperature and pH conditions, shear stress, antimicrobial agents, and
other environmental perturbations (1). Mature biofilms are mixed microbial communities
comprising algal, fungal, and/or protozoan species in addition to bacteria. The matrix of
extracellular polymeric substances (EPS) that keeps the bacterial cells together confers re-
silience and versatility to biofilms by mediating nutrient and water transport, regulating
metabolism, offering protection against antibiotics and disinfectants, helping in cell-cell
communication, and influencing predator-prey interactions (2). This successful community
lifestyle of bacteria has gained research interest, especially since the dawn of the biotech-
nology revolution. From an anthropocentric perspective, biofilms can be detrimental or
beneficial.
Biofilms have been implicated in chronic infections that seldom respond to antibi- Editor Hideaki Nojiri, University of Tokyo
otic treatment (3, 4). The involvement of biofilms in food spoilage (5) has led to the de- Copyright © 2022 American Society for
Microbiology. All Rights Reserved.
velopment of approaches that employ interventions involving physicochemical altera-
Address correspondence to A. S.
tion of surfaces and addition of biochemical agents to disrupt cell-cell communication Vishwanathan, [email protected].
(6). On the other hand, biofilms are central to microbial biotransformations for the The authors declare no conflict of interest.
industrial production of commercially valuable products, such as enzymes, antibiot- This work is dedicated to Bhagawan Sri Sathya
ics, and secondary metabolites (7). Biotrickling filters capitalize on multispecies bio- Sai Baba, the founder chancellor of the Sri
Sathya Sai Institute of Higher Learning.
films for remediation of polluted air and water and in the treatment of contaminated
Accepted manuscript posted online
soils by bioaugmentation and biostimulation (8). Biofilms comprising electrochemi- 1 December 2021
cally active bacteria have been exploited for energy and resource recovery from Published 8 February 2022
wastewater (9).

February 2022 Volume 88 Issue 3 e01994-21 Applied and Environmental Microbiology aem.asm.org 1
Minireview Applied and Environmental Microbiology

A deeper understanding of the formation, progression, and dispersion of biofilms is


essential for developing strategies to promote their growth for beneficial applications.
Several approaches have been considered to manipulate biofilm growth and function.
Among them, the addition of biochemical agents that induce physiologic stress by
interfering with signaling molecules and quorum-sensing (QS) pathways critical to bio-
film formation (10, 11), the chemical modification of the substratum that the biofilms
colonize to promote aggregation and adhesion (12), and manipulation of genes
involved in the subsistence of biofilms to either upregulate or downregulate them
based on their function (13) are noteworthy. This information is available but spread
out in research articles across journals in diverse domains such as health care and vet-
erinary medicine, food science and agriculture, and environmental sciences, including
water research and environmental engineering. Several of these areas consider bio-
films a health hazard and describe means to prevent their formation and to eliminate
them. In contrast, this minireview consolidates different approaches to enhance biofilm
formation and provides directions for furthering these developments. The examples
provided in this article showcase strategies that have been successfully employed to
this end and are by no means exhaustive.

MODIFYING THE EXTERNAL ENVIRONMENT


Planktonic and biofilm bacteria are sensitive to changes in their surroundings.
Subjecting a mixed culture of bacteria to nonoptimal pH and temperature conditions
accelerated biofilm formation and enhanced their electroactivity in microbial electro-
chemical systems (14, 15). Nutrient deprivation is among the most severe kinds of
stress that an organism can encounter. Limiting the availability of nutrients is a simple
yet effective method that can be used to trigger the formation of biofilms (16).
An initial step associated with development of a biofilm is the attachment of bacte-
rial cells to a surface. Studies conducted using different microtiter plate materials
showed that surface chemistry profoundly impacts Staphylococcus biofilm formation
(17). Chemical treatment of a surface by the addition or removal of specific functional
groups can bring about changes in the hydrophobicity and surface charge, thereby
stimulating biofilm formation (18–20). Treatment of the carbon felt anode of a micro-
bial fuel cell by exposure to UV rays and ozone gas promoted the attachment of

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Shewanella oneidensis MR-1 biofilms, resulting in increased current generation (21).
Sarjit et al. (19) described different surface modifications that have been used to
enhance biofilm formation in specific applications, such as fermentation, bioremedia-
tion, biosensing, and energy recovery, in bioelectrochemical systems. There is scope
for enhancing the efficiency of such applications by synthesizing novel low-cost, bio-
compatible materials that facilitate the attachment of bacterial cells to a surface result-
ing in increased biofilm formation (22, 23). Additionally, modifying the surface topogra-
phy on a microscale or below also has the potential to positively impact bacterial
colonization and the performance of electroactive biofilms (24, 25).
Following their attachment to the surface, bacterial cells start aggregating and
enclose themselves in a self-produced matrix of extracellular polymeric substances
(26). Acinetobacter baumannii and Klebsiella pneumoniae grown in the presence of
long-chain polyunsaturated fatty acids significantly increased biofilm formation (27,
28). Simple carbohydrates such as glucose, glucosamine, and N-acetylglucosamine
enhanced EPS production in Staphylococcus aureus, Listeria monocytogenes, and
Streptococcus mutans (29, 30). Addition of divalent cations such as Ca21 and Mg21 posi-
tively influenced biofilm formation in Pseudomonas spp. by forming electrostatically
mediated cross-links within the matrix to maintain cohesive forces between the bacte-
rial cells (31). Studies on Gram-negative bacteria such as Shigella boydii and Salmonella
enterica serovar Typhimurium have shown that salt stress can trigger increased adhe-
sion of cells to a surface (32). It can be gathered from these reports that the physical
processes associated with the attachment and aggregation of bacterial cells present
many opportunities for introducing interventions to improve biofilm formation.

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Minireview Applied and Environmental Microbiology

SUPPLYING ELICITORS AND SIGNALING MOLECULES


Changes in the external environment often set off a series of signaling pathways in
bacteria that proceed to regulate genes associated with biofilm formation (33).
Communication channels within a biofilm serve as a lifeline for its maintenance and
modulation (34, 35). Exogenously supplied biochemical compounds that modify bio-
film development pathways have shown great promise in fostering the development
of biofilms (11, 36).
Different classes of antibiotics, used globally to tackle bacterial infections, when
applied in a dose-dependent manner at subinhibitory concentrations can increase the
production of biofilms through the modulation of biofilm-signaling genes (QS and c-
di-GMP), EPS synthesis genes, and other virulence genes involved in biofilm develop-
ment (36, 37). Zhou et al. (38) used tobramycin in the anode chamber of a microbial
fuel cell at 1/80 MIC and 1/40 MIC to enhance the electroactive biofilm mass by about
50%, resulting in a quicker start-up time and a significant increase in the current den-
sity. Transcriptomic analysis correlated this improvement with the upregulation of
genes encoding type 4 pili and c-type cytochromes (38). However, extreme caution
must be exercised in the use of antibiotics at subinhibitory concentrations due to the
emergence of antimicrobial resistance as a global public threat (https://www.who.int/
news-room/fact-sheets/detail/antimicrobial-resistance).
In many Gram-negative bacteria, the QS system functions as a cell-to-cell communi-
cation network that regulates formation of the biofilm matrix through the action of
autoinducer molecules (39). N-acylhomoserine lactone (AHL) type autoinducers with
long acyl chains positively modulated biofilms formed by the bioleaching bacterium
Acidithiobacillus ferrooxidans by increasing EPS synthesis and improving the adhesion
of bacterial cells to the substratum (10, 40). Trace levels of the Pseudomonas aeruginosa
QS signal (PQS) and 4-hydroxy-1-methyl-2-quinolone autoinducer enhanced the power
density of a hypersaline microbial fuel cell by increasing the anodic biofilm mass of the
extremophile Halanaerobium praevalens through elevated expression of polysaccha-
ride biosynthesis genes (11).
Addition of quinones and flavins, which act as electron mediators in a bioelectrochemi-
cal system, enhanced S. oneidensis MR-1 biofilms and contributed to higher current den-
sities (41). Das and Manefield (42) reported that pyocyanin triggers the release of extracel-

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lular DNA, which is known to play a pivotal role in the establishment and stability of
biofilms in a number of bacterial species, such as P. aeruginosa and S. oneidensis MR-1. In
an interesting finding, Zhang et al. (43) demonstrated that the addition of low concentra-
tions of lytic polyvalent bacteriophages to bacterial cultures could serve as a stress-related
trigger to stimulate biofilm growth by upregulating QS genes, EPS biosynthesis genes, and
curli production genes in Escherichia coli and P. aeruginosa.
This approach of augmenting biofilm formation by exogenous addition of effectors
and signaling molecules requires a comprehensive understanding of the molecular
pathways associated with biofilm formation. A quick glance at the biofilm formation
pathways of model systems, such as P. aeruginosa and E. coli, available in the Kyoto
Encyclopedia of Genes and Genomes (KEGG) database (https://www.genome.jp/kegg/),
reveals the complexity of the interlinkages across multiple biochemical processes. A
detailed cross-species analysis is needed to obtain a clearer picture of the biofilm-regu-
lating proteins and pathways that have been conserved. The outcome of such a study
could facilitate the identification of molecules that can then be supplied exogenously to
alter the performance of those key proteins. A large number of secondary metabolites
from plants and fungi are continually being tested and reported for their antimicrobial
potential and antibiofilm activity as alternatives to conventional antibiotics (44, 45). It is
worth investigating the effectiveness of subinhibitory concentrations of these metabo-
lites in enhancing biofilm formation. Exploratory studies using different phenazine com-
pounds, which are known to release reactive oxygen species, could help in formulating
approaches to promote biofilm formation (46, 47).

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A recent study describing an in silico approach to screen and identify chemical com-
pounds that have the potential to promote biofilm formation by inhibiting previously
identified biofilm-antagonistic proteins highlights the scope of computational biology in
this regard (48). However, further experimental studies are needed to validate the in vitro
efficacy of these compounds. The availability of crystallized protein structures in the
Protein Data Bank (https://www.rcsb.org/) and curated databases of chemical ligands
such as PubChem (https://pubchem.ncbi.nlm.nih.gov/), ZINC (http://zinc.docking.org/)
(for chemical compounds), COCONUT (https://coconut.naturalproducts.net/) (for natural
products), and ChEMBL (https://www.ebi.ac.uk/chembl/) (for bioactive molecules with
drug-like properties) has simplified the virtual screening process. This is an alternative
approach to work out the feasibility of enhancing biofilms by exogenously supplying
biofilm-promoting compounds.

ENGINEERING GENES ASSOCIATED WITH BIOFILM FORMATION


Knowledge of the molecular mechanisms involved in the development and regula-
tion of biofilms opens up the route to genetically manipulate cells by overexpression
of biofilm-promoting genes, heterologous gene expression, or mutagenesis to disrupt
biofilm-antagonistic proteins. Cyclic di-GMP (commonly known as c-di-GMP or cyclic
diguanylate), a second messenger that plays a crucial role in the transition of plank-
tonic bacteria into biofilm-forming bacteria, is an attractive target for genetic engineer-
ing (49). A high intracellular concentration of c-di-GMP leads to increased biofilm for-
mation by inducing sessility and activating the synthesis of adhesins and EPS, while
lower concentrations trigger motility and biofilm dispersion (49). Overexpression of
vdeH (a c-di-GMP gene) and cyclic AMP synthase genes in S. oneidensis promoted bio-
film formation and enhanced the performance of bioelectrochemical systems (49). Wu
et al. (50) constitutively expressed yedQ (a c-di-GMP synthase gene from E. coli) in
Comamonas testosteroni, which led to enhanced biofilm formation and consequently
improved the degradation of 3-chloroaniline, a recalcitrant organic pollutant found in
herbicide-treated soils. Directed evolution via random mutagenesis led to a more effi-
cient version of SdiA protein (a key QS probiofilm regulator) that resulted in a 7-fold
increase in E. coli biofilm formation (51).
Disruption of a putrescine biosynthesis gene (speF) implicated in mediating the dis-

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assembly of biofilm matrices increased the EPS content and resulted in a hyperadher-
ent strain of S. oneidensis with enhanced capacity to immobilize the toxic heavy-metal
contaminant chromate(VI) from an aqueous phase (52). Mutation of BifA (the gene
encoding a phosphodiesterase enzyme that degrades c-di-GMP in P. aeruginosa)
enriched the levels of intracellular c-di-GMP, elevated Pel polysaccharide synthesis, and
enhanced biofilm formation (53). Mutants of tpbA (which encodes a QS-associated
phosphatase that negatively regulates c-di-GMP concentration in P. aeruginosa) dis-
played an increase in biofilm formation by about 150 times, resulting from a rise in the
production of Pel and Psl polysaccharides and a reduction in swarming behavior of
cells due to higher intracellular concentrations of c-di-GMP (54).
Despite all the progress that has been made in biofilm engineering, this field is still
said to be in the nascent stages of the learning curve (49). Two important aspects to
be considered while working with genetically modified bacteria for environmental
applications are the cost-effectiveness of the process and the risks arising from the
release of such organisms into nature.

CONCLUSIONS
This article presents a summary of different approaches adopted to enhance biofilm
formation with the objective of improving the efficiency of microbe-catalyzed biotech-
nological processes. The simplest of the techniques for promoting the formation of
biofilms involves subjecting bacterial cells to controlled physiological stress that causes
them to aggregate and attach firmly to a substratum more effectively. Biofilm forma-
tion can be enhanced by exogenously supplementing biochemical elicitors that

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augment the signaling cascades responsible for the maintenance of a biofilm. The final
approach involving the manipulation of genes encoding biofilm-associated proteins
demands a significant amount of sophistication and finesse, which can inflate the asso-
ciated costs. A prudent combination of the physicochemical, biological, and computa-
tional approaches outlined in the article will have to be worked out to enhance biofilm
development and activity for specific applications. Taking a cue from the quote attrib-
uted to Aristophanes, an ancient Greek playwright, “The wise learn many things from
their enemies,” the ingenious strategies devised to dislodge and degrade biofilms
might, in fact, hold many secrets to establish and promote them.

ACKNOWLEDGMENTS
We are grateful for the valuable comments provided during the peer review process,
which substantially improved the quality of the manuscript.

REFERENCES
1. Tallawi M, Opitz M, Lieleg O. 2017. Modulation of the mechanical proper- microbial electrochemical technologies. Biotechnol Adv 39:107468.
ties of bacterial biofilms in response to environmental challenges. Bio- https://doi.org/10.1016/j.biotechadv.2019.107468.
mater Sci 5:887–900. https://doi.org/10.1039/c6bm00832a. 16. D’Souza GG, Povolo VR, Keegstra JM, Stocker R, Ackermann M. 2021. Nutri-
2. Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. ent complexity triggers transitions between solitary and colonial growth in
2016. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14: bacterial populations. ISME J 15:2614–2623. https://doi.org/10.1038/s41396
563–575. https://doi.org/10.1038/nrmicro.2016.94. -021-00953-7.
3. Vestby LK, Grønseth T, Simm R, Nesse LL. 2020. Bacterial biofilm and its 17. Kennedy CA, O'Gara JP. 2004. Contribution of culture media and chemical
role in the pathogenesis of disease. Antibiotics 9:59. https://doi.org/10 properties of polystyrene tissue culture plates to biofilm development by
.3390/antibiotics9020059. Staphylococcus aureus. J Med Microbiol 53:1171–1173. https://doi.org/10
4. Sharma D, Misba L, Khan AU. 2019. Antibiotics versus biofilm: an emerg- .1099/jmm.0.45764-0.
ing battleground in microbial communities. Antimicrob Resist Infect Con- 18. Santoro C, Arbizzani C, Erable B, Ieropoulos I. 2017. Microbial fuel cells: from
trol 8:1–10. https://doi.org/10.1186/s13756-019-0533-3. fundamentals to applications. A review. J Power Sources 356:225–244.
5. Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A. 2021. Microbial https://doi.org/10.1016/j.jpowsour.2017.03.109.
biofilms in the food industry—a comprehensive review. IJERPH 18:2014. 19. Sarjit A, Mei Tan S, A Dykes G. 2015. Surface modification of materials to
https://doi.org/10.3390/ijerph18042014. encourage beneficial biofilm formation. AIMS Bioeng 2:404–422. https://
6. Yuan L, Hansen MF, Røder HL, Wang N, Burmølle M, He G. 2020. Mixed- doi.org/10.3934/bioeng.2015.4.404.
species biofilms in the food industry: current knowledge and novel con- 20. Li C, Cheng S. 2019. Functional group surface modifications for enhancing
trol strategies. Crit Rev Food Sci Nutr 60:2277–2293. https://doi.org/10 the formation and performance of exoelectrogenic biofilms on the anode
.1080/10408398.2019.1632790. of a bioelectrochemical system. Crit Rev Biotechnol 39:1015–1030.
7. Germec M, Demirci A, Turhan I. 2020. Biofilm reactors for value-added https://doi.org/10.1080/07388551.2019.1662367.
products production: an in-depth review. Biocatal Agric Biotechnol 27: 21. Cornejo JA, Lopez C, Babanova S, Santoro C, Artyushkova K, Ista L, Schuler
101662. https://doi.org/10.1016/j.bcab.2020.101662. AJ, Atanassov P. 2015. Surface modification for enhanced biofilm forma-
8. Ali N, Dashti N, Khanafer M, Al-Awadhi H, Radwan S. 2020. Bioremediation tion and electron transport in Shewanella anodes. J Electrochem Soc 162:
H597–H603. https://doi.org/10.1149/2.0271509jes.

Downloaded from https://journals.asm.org/journal/aem on 17 March 2024 by 41.200.108.251.


of soils saturated with spilled crude oil. Sci Rep 10:1–9. https://doi.org/10
22. Zhang X, Zhou X, Ni H, Rong X, Zhang Q, Xiao X, Huan H, Liu JF, Wu Z.
.1038/s41598-019-57224-x.
2018. Surface modification of basalt fiber with organic/inorganic compo-
9. Kiran R, Patil SA. 2019. Microbial electroactive biofilms, p 159–186. In
sites for biofilm carrier used in wastewater treatment. ACS Sustainable
Rathinam NK, Sani RK (ed), Introduction to biofilm engineering. American
Chem Eng 6:2596–2602. https://doi.org/10.1021/acssuschemeng.7b04089.
Chemical Society, Washington, DC.
23. Chen X, Li Y, Yuan X, Li N, He W, Feng Y, Liu J. 2020. Surface modification
10. González A, Bellenberg S, Mamani S, Ruiz L, Echeverría A, Soulère L,
by b -cyclodextrin/polyquaternium-11 composite for enhanced biofilm
Doutheau A, Demergasso C, Sand W, Queneau Y, Vera M, Guiliani N. 2013.
formation in microbial fuel cells. J Power Sources 480:228789. https://doi
AHL signaling molecules with a large acyl chain enhance biofilm forma-
.org/10.1016/j.jpowsour.2020.228789.
tion on sulfur and metal sulfides by the bioleaching bacterium Acidithio-
24. Champigneux P, Delia ML, Bergel A. 2018. Impact of electrode micro- and
bacillus ferrooxidans. Appl Microbiol Biotechnol 97:3729–3737. https:// nano-scale topography on the formation and performance of microbial
doi.org/10.1007/s00253-012-4229-3. electrodes. Biosens Bioelectron 118:231–246. https://doi.org/10.1016/j
11. Monzon O, Yang Y, Li Q, Alvarez PJJ. 2016. Quorum sensing autoinducers .bios.2018.06.059.
enhance biofilm formation and power production in a hypersaline microbial 25. Dolid A, Gomes LC, Mergulhão FJ, Reches M. 2020. Combining chemistry
fuel cell. Biochem Eng J 109:222–227. https://doi.org/10.1016/j.bej.2016.01 and topography to fight biofilm formation: fabrication of micropatterned
.023. surfaces with a peptide-based coating. Colloids Surf B Biointerfaces 196:
12. Xiao N, Wu R, Huang JJ, Selvaganapathy PR. 2020. Anode surface modifi- 111365. https://doi.org/10.1016/j.colsurfb.2020.111365.
cation regulates biofilm community population and the performance of 26. Watnick P, Kolter R. 2000. Biofilm, city of microbes. J Bacteriol 182:
micro-MFC based biochemical oxygen demand sensor. Chem Eng Sci 2675–2679. https://doi.org/10.1128/JB.182.10.2675-2679.2000.
221:115691. https://doi.org/10.1016/j.ces.2020.115691. 27. Eder AE, Munir SA, Hobby CR, Anderson DM, Herndon JL, Siv AW, Symes
13. Hu Y, Mukherjee M, Cao B. 2019. Biofilm-biology-informed biofilm engi- SJK, Giles DK. 2017. Exogenous polyunsaturated fatty acids (PUFAs) alter
neering for environmental biotechnology, p 59–82. In Rathinam NK, Sani phospholipid composition, membrane permeability, biofilm formation
RK (ed) Introduction to biofilm engineering. American Chemical Society, and motility in Acinetobacter baumannii. Microbiology (Reading) 163:
Washington, DC. 1626–1636. https://doi.org/10.1099/mic.0.000556.
14. Patil SA, Harnisch F, Koch C, Hübschmann T, Fetzer I, Carmona-Martínez 28. Hobby CR, Herndon JL, Morrow CA, Peters RE, Symes SJK, Giles DK. 2019.
AA, Müller S, Schröder U. 2011. Electroactive mixed culture derived biofilms Exogenous fatty acids alter phospholipid composition, membrane per-
in microbial bioelectrochemical systems: the role of pH on biofilm forma- meability, capacity for biofilm formation, and antimicrobial peptide sus-
tion, performance and composition. Bioresour Technol 102:9683–9690. ceptibility in Klebsiella pneumoniae. Microbiologyopen 8:e00635-11.
https://doi.org/10.1016/j.biortech.2011.07.087. https://doi.org/10.1002/mbo3.635.
15. Chiranjeevi P, Patil SA. 2020. Strategies for improving the electroactivity 29. She P, Wang Y, Liu Y, Tan F, Chen L, Luo Z, Wu Y. 2019. Effects of exoge-
and specific metabolic functionality of microorganisms for various nous glucose on Pseudomonas aeruginosa biofilm formation and

February 2022 Volume 88 Issue 3 e01994-21 aem.asm.org 5


Minireview Applied and Environmental Microbiology

antibiotic resistance. Microbiologyopen 8:933. https://doi.org/10.1002/ 43. Zhang B, Yu P, Wang Z, Alvarez PJJ. 2020. Hormetic promotion of biofilm
mbo3.933. growth by polyvalent bacteriophages at low concentrations. Environ Sci
30. Brito ACM, Bezerra IM, de Borges MHS, Cavalcanti YW, de de Almeida LFD. Technol 54:12358–12365. https://doi.org/10.1021/acs.est.0c03558.
2021. Effect of different salivary glucose concentrations on dual-species 44. Lahiri D, Dash S, Dutta R, Nag M. 2019. Elucidating the effect of anti-bio-
biofilms of Candida albicans and Streptococcus mutans. Biofouling 37: film activity of bioactive compounds extracted from plants. J Biosci 44:
615–625. https://doi.org/10.1080/08927014.2021.1946519. 1–19. https://doi.org/10.1007/s12038-019-9868-4.
31. Song B, Leff LG. 2006. Influence of magnesium ions on biofilm formation 45. Lu L, Hu W, Tian Z, Yuan D, Yi G, Zhou Y, Cheng Q, Zhu J, Li M. 2019. Devel-
by Pseudomonas fluorescens. Microbiol Res 161:355–361. https://doi.org/ oping natural products as potential anti-biofilm agents. Chinese Med 14:
10.1016/j.micres.2006.01.004. 1–17.
32. Xu H, Zou Y, Lee H-Y, Ahn J. 2010. Effect of NaCl on the Biofilm Formation 46. Das T, Kutty SK, Tavallaie R, Ibugo AI, Panchompoo J, Sehar S, Aldous L,
by Foodborne Pathogens. J Food Sci 75:M580–M585. https://doi.org/10
Yeung AWS, Thomas SR, Kumar N, Gooding JJ, Manefield M. 2015. Phena-
.1111/j.1750-3841.2010.01865.x.
zine virulence factor binding to extracellular DNA is important for Pseu-
33. Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, Nomura N. 2016.
domonas aeruginosa biofilm formation. Sci Rep 5:1–9. https://doi.org/10
Environmental factors that shape biofilm formation. Biosci Biotechnol
Biochem 80:7–12. https://doi.org/10.1080/09168451.2015.1058701. .1038/srep08398.
34. Wilking JN, Zaburdaev V, De Volder M, Losick R, Brenner MP, Weitz DA. 47. Gambino M, Cappitelli F. 2016. Mini-review: biofilm responses to oxida-
2013. Liquid transport facilitated by channels in Bacillus subtilis biofilms. tive stress. Biofouling 32:167–178. https://doi.org/10.1080/08927014
Proc Natl Acad Sci U S A 110:848–852. https://doi.org/10.1073/pnas .2015.1134515.
.1216376110. 48. Mukhi M, Vishwanathan AS. 21 September 2021. Identifying potential
35. Prindle A, Liu J, Asally M, Ly S, Garcia-Ojalvo J, Süel GM. 2015. Ion channels inhibitors of biofilm-antagonistic proteins to promote biofilm formation:
enable electrical communication in bacterial communities. Nature 527: a virtual screening and molecular dynamics simulations approach. Mol
59–63. https://doi.org/10.1038/nature15709. Divers https://doi.org/10.1007/s11030-021-10320-5.
36. Kaplan JB, Izano EA, Gopal P, Karwacki MT, Kim S, Bose JL, Bayles KW, 49. Mukherjee M, Cao B. 2021. Engineering controllable biofilms for biotech-
Horswill AR. 2012. Low levels of b -lactam antibiotics induce extracellular nological applications. Microb Biotechnol 14:74–78. https://doi.org/10
DNA release and biofilm formation in Staphylococcus aureus. mBio 3:2–9. .1111/1751-7915.13715.
https://doi.org/10.1128/mBio.00198-12. 50. Wu Y, Ding Y, Cohen Y, Cao B. 2015. Elevated level of the second messen-
37. Kaplan JB. 2011. Antibiotic-induced biofilm formation. Int J Artif Organs ger c-di-GMP in Comamonas testosteroni enhances biofilm formation
34:737–751. https://doi.org/10.5301/ijao.5000027. and biofilm-based biodegradation of 3-chloroaniline. Appl Microbiol Bio-
38. Zhou L, Li T, An J, Liao C, Li N, Wang X. 2017. Subminimal inhibitory con- technol 99:1967–1976. https://doi.org/10.1007/s00253-014-6107-7.
centration (sub-MIC) of antibiotic induces electroactive biofilm formation 51. Lee J, Maeda T, Hong SH, Wood TK. 2009. Reconfiguring the quorum-sens-
in bioelectrochemical systems. Water Res 125:280–287. https://doi.org/10 ing regulator sdiA of escherichia coli to control biofilm formation via indole
.1016/j.watres.2017.08.059. and N-acylhomoserine lactones. Appl Environ Microbiol 75:1703–1716.
39. Yu M, Chua SL. 2020. Demolishing the great wall of biofilms in Gram-neg-
https://doi.org/10.1128/AEM.02081-08.
ative bacteria: to disrupt or disperse? Med Res Rev 40:1103–1116. https://
52. Ding Y, Peng N, Du Y, Ji L, Cao B. 2014. Disruption of putrescine biosyn-
doi.org/10.1002/med.21647.
thesis in Shewanella oneidensis enhances biofilm cohesiveness and per-
40. Wang J, Liu Q, Dong D, Hu H, Wu B, Ren H. 2021. AHLs-mediated quorum
sensing threshold and its response towards initial adhesion of waste- formance in Cr(VI) immobilization. Appl Environ Microbiol 80:1498–1506.
water biofilms. Water Res 194:116925. https://doi.org/10.1016/j.watres https://doi.org/10.1128/AEM.03461-13.
.2021.116925. 53. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, O'Toole GA.
41. Wu Y, Luo X, Luo X, Luo X, Qin B, Li F, Häggblom MM, Liu T, Liu T. 2020. 2007. BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm
Enhanced current production by exogenous electron mediators via synergy formation and swarming motility by Pseudomonas aeruginosa PA14. J
of promoting biofilm formation and the electron shuttling process. Environ Bacteriol 189:8165–8178. https://doi.org/10.1128/JB.00586-07.
Sci Technol 54:7217–7225. https://doi.org/10.1021/acs.est.0c00141. 54. Ueda A, Wood TK. 2010. Tyrosine phosphatase TpbA of Pseudomonas
42. Das T, Manefield M. 2012. Pyocyanin promotes extracellular DNA release aeruginosa controls extracellular DNA via cyclic diguanylic acid concen-

Downloaded from https://journals.asm.org/journal/aem on 17 March 2024 by 41.200.108.251.


in Pseudomonas aeruginosa. PLoS One 7:e46718. https://doi.org/10 trations. Environ Microbiol Rep 2:449–455. https://doi.org/10.1111/j.1758
.1371/journal.pone.0046718. -2229.2010.00171.x.

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