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Multispecies Interactions in Biofilms and Implications to Safety of Drinking

Water Distribution System

Article  in  Korean Journal of Microbiology and Biotechnology · December 2019

DOI: 10.4014/mbl.1907.07007

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 Microbiol. Biotechnol. Lett. (2019), 47(4), 473–486
http://dx.doi.org/10.4014/mbl.1907.07007
pISSN 1598-642X eISSN 2234-7305
Microbiology and Biotechnology Letters

Review

Multispecies Interactions in Biofilms and Implications

to Safety of Drinking Water Distribution System
Rine Christopher Reuben1,2, Pravas Chandra Roy1, Shovon Lal Sarkar1, Sang-Do Ha3, and Iqbal Kabir Jahid1*
1
Department of Microbiology, Jashore University of Science and Technology, Jashore-7408, Bangladesh
2
Department of Science Laboratory Technology, Nasarawa State Polytechnic, Lafia, Nigeria
3
School of Food Science and Technology, Chung-Ang University, Ansung 17546, Republic of Korea

Received: July 15, 2019 / Revised: September 6, 2019 / Accepted: September 6, 2019

In the aquatic environment, microorganisms are predominantly organized as biofilms. Biofilms are formed
by the aggregation of microbial cells and are surrounded by a matrix of extracellular polymeric substances
(EPS) secreted by the microbial cells. Biofilms are attached to various surfaces, such as the living tissues,
indwelling medical devices, and piping of the industrial potable water system. Biofilms formed from a sin-
gle species has been extensively studied. However, there is an increased research focus on multispecies bio-
films in recent years. It is important to assess the microbial mechanisms underlying the regulation of
multispecies biofilm formation to determine the drinking water microbial composition. These mechanisms
contribute to the predominance of the best-adapted species in an aquatic environment. This review focuses
on the interactions in the multispecies biofilms, such as coaggregation, co-metabolism, cross-species pro-
tection, jamming of quorum sensing, lateral gene transfer, synergism, and antagonism. Further, this review
explores the dynamics and the factors favoring biofilm formation and pathogen transmission within the
drinking water distribution systems. The understanding of the physiology and biodiversity of microbial
species in the biofilm may aid in the development of novel biofilm control and drinking water disinfection
processes.

Keywords: Multispecies, biofilm, water, disease, biodiversities

Introduction majority of people have inadequate access to safe water

in spite of the United Nations effort in improving water
Water is one major and essential need of all humans, quality [2]. It is of significant importance also to note
as such, it should be readily accessible, safe and ade- that there is a direct relationship between disease burden
quately supply to all. Unfortunately, high populations of and water quality. As such, global disease burden can be
people globally do not have access to purified water reduced by approximately 4 percent by improving water
sources, thereby constituting a grave sanitation conse- quality [1]. Globally, it is suggested that waterborne
quence. The impact of poor hygiene and sanitation as a diseases have an estimated economic cost of nearly $12
result of the consumption of unsafe water results in an billion annually while about $1 billion is annually spent
estimated 3.2 percent death globally [1]. It is highly per- in the United States alone [3].
tinent to note that in most developing countries, the In nature, microorganisms rarely exist as planktonic
or free-living cells. They are largely found in enclosed
*Corresponding author
matrix, forming complex communities [4]. Despite this,
Tel: +88-01709-818127
E-mail: [email protected] most of the biofilm research has extensively focused on
© 2019, The Korean Society for Microbiology and Biotechnology in vitro mono-cultures biofilm formation [5]. Only more

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474 Reuben et al.

recently has the focus been moved toward the under- [6]. In nature, about 99 percent of bacteria exist in biofilms
standing of microbial diversity and interaction in the while 65 percent of infections in the hospital are
natural environment. Furthermore, the increased dis- attributed to biofilms [8]. When in biofilms, bacteria
coveries of the unique metabolic capabilities of microbial usually show profound differences in both morphological
communities have drawn more interest to microbial life- and physiological features vis-à-vis planktonic cultures.
style in natural ecosystems [4]. This has unraveled Some of the most profound features of bacteria in bio-
emergent microbial properties not previously detected in films include resistance to unfavorable environmental
free-living cells. factors; desiccation, pollutants, antimicrobial agents (in
Microorganisms readily attach to diverse surfaces and nature), host defenses, and protozoan grazing [9, 10].
subsequently form biofilms in aquatic environments. The presence of biofilms containing pathogens such as
The impact of biofilm formation in medicine, changing Aeromonas spp, Escherichia coli, and Pseudomonas spp.
antimicrobial therapeutics and comprehension of in drinking water constitute a great potential risk to
chronic and emerging infections has been tremendous in public health [11]. This is because biofilms can contain a
recent times. Despite the intensive research on this very high number of microbial cells, up to 1.0 × 109 per
topic, the impact of biofilm on ecosystems, and more clump, capable of causing infections when ingested.
specifically, in the aquatic environment has not been However, little is known on bacterial survival and poten-
given the same importance. In aquatic ecosystems, tiality to cause disease in biofilms.
biofilms have been recognized as the predominant forms
of life due to innumerable benefits bacterial interactions Multispecies Biofilms
within this matrix provide.
This review describes the various interactions in mul- Mixed microbial populations exist in different niches
tispecies biofilms including coaggregation of microbial (including aquatic systems), having distinct phenotypic
cells, cross-species interaction, and co-metabolism, lateral variants which have a significant effect on the overall
gene transfer, jamming of quorum sensing, synergism activities of microbial communities in biofilm [12].
and antagonism. We also provide updates on the role of Bacteria attach to such surfaces either as discrete and
biofilms in disease transmission and dynamics, their separate individual cells, aggregates or biofilm com-
influence on distribution systems of drinking water, and munities interacting with other cells thereby forming
finally the effects of protozoan grazing on aquatic bio- channels for both nutrients and metabolic by-products
films. circulation which often exists as a three-dimensional
architectural structure [13]. Multispecies biofilm can
Biofilms solely comprise of single individual microbial strains or
multiple strains within a habitat [8]. The diversity of
Donlan and Costerton [6] defined biofilm as a com- population reduces the impact of environmental stress
munity of microorganisms adhering to biotic or abiotic because wide range of environmental conditions are
surfaces and embedded with a self-produced extracellular extended for the survival of different microbial subpopu-
polymeric substances (EPS) which facilitate survival in lations within their community. Different physiological
an adverse environment. Biofilms can also be seen as and regulatory alterations occur with multispecies bio-
complex architectural assemblies of microorganisms on films as a result of microbial interactions. This eventually
or in biotic and abiotic surfaces and interfaces, charac- favors the selection and survival of the most adapted
terized by interactions between populations. They have strains or mutants. Consequently, these aid in shaping
survived as self-organized, three-dimensional structures multispecies biofilm communities as certain species may
that exhibit altered genotypic and phenotypic character- eventually emerge or disappear.
istics [7]. The ubiquity nature of biofilms enables them Recently, we reviewed the roles played by multispecies
to thrive and survive in different water systems (includ- biofilms with regards to food safety, where we provided
ing aquatic and industrial), environments and devices detailed interactions and the importance of multispecies
(medical) which are of great public health importance biofilms in foods [7]. Multispecies biofilms generally

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 Multispecies Biofilms and Drinking Water Safety 475

show more resistance to disinfectants because they gravel and cobbles) are referred to as epilithic biofilms or
secrete more EPS compared with mono-species biofilms. epilithon in rivers, marine environments and lakes [17].
Unlike biofilms formed on other substrata, epilithic
Characteristics of Biofilms in Aquatic biofilms have a more complex structure with higher
Environments algal biomass and are more independent on seasonal
fluctuations [18].
Microbial communities existing as biofilms are rarely Stones provide a three-dimensional physical habitat
planktonic in the aquatic environment. They adhere to for biofilm biomass. The developing biofilms are greatly
different surfaces of living tissues, dead matter or influenced by rock characteristics such as surface
devices which prevent them from external forces capable texture, stone size, and stone orientation [19]. On the
of sweeping them away [14]. When attached to a surface, one hand, a rougher surface can cause greater biofilm
Pseudomonas aeruginosa biofilm often produces an accumulation on rocks since it increases the sedimenta-
exopolysaccharide known as alginate, which serves as tion efficiency and cell adhesion and further protects the
an extracellular matrix. Also, V. cholera producing this biofilm from disturbances such as scouring and grazing
same exopolymer barrier form biofilms on different [19]. On the other hand, stone size and stability
surfaces (both biotic and abiotic), which provides protec- determine the algal resistance to scour. Regarding stone
tion to the cells. V. cholerae also forms a rugose colony in orientation, horizontal surfaces consistently harbor
multispecies biofilms isolated from Ganges Delta, more biofilm than on vertical surfaces [19]. Biofilms
Bangladesh [13]. developing on rocks have structural stability and close
Furthermore, within the aquatic environments, bio- spatial relationship between bacteria and algae favor
films can be highly diverse depending on the substratum the bacterial use of fresh labile organic compounds
where they develop. In natural environments, biofilms released by algae, which affect the metabolism of the
grow upon inert substrata such as sand, sediment, rocks whole biofilm.
and cobbles; non-living organic substrata such as wood,
leaf litter or particular organic matter; and living plants Sediment. Microorganisms attached to sand and
such as aquatic macrophytes and macroalgae [15]. gravel (sandy sediments) are referred to as epipsammic,
Multispecies biofilms composition, structure, diversity while when developing on muddy sediments (clay or silt)
and metabolism are largely determined by the nature they are known as epipelic [20]. Sediments are usually
and kind of substratum such communities are formed. hard and inert substrata with a smaller size than other
Furthermore, it has been demonstrated that substratum substrates. In rivers, biofilms developing on sediment
properties which support biofilms development also play key role especially in the decomposition of organic
determine cells accumulation patterns especially in the matter and are also highly heterotrophic when compared
early stages of biofilms formation [16]. Table 1 shows the to rock biofilms.
multispecies biofilm growth in different substratum. Colonization and microbial community development
on sediments depend on the roughness, size and surface
Rocks. Biofilms attached to rock surfaces (also to area of the grains. Specifically, microbial colonization on

Table 1. Biofilm growth in substratum.

S/N Organism (s) Substratum of biofilm formation References
1 Heterotrophic bacteria, fungi and protozoa Rocks 16, 21
2 Cyanobacteria, euglenids and diatoms Sediments 21, 38
3 Bacteria, archaea, algae and metazoans Dead plant Material 20, 23,
4 Bacteria and algae Living plants 29, 30
5 Cyanobacteria, bacteria and protozoans Suspended aggregates 29-31
6 Gram-positive bacteria and diatoms Man-made surfaces 34, 36

December 2019 | Vol. 47 | No. 4

476 Reuben et al.

sediment grains is proportional to the grain surface the decomposition velocity may be very important for
area. However, these assumptions can be applied only biofilm development since slower decomposition enables
from coarse grains to fine silt because clay particles are the organic substrate to remain in the system longer
very rarely colonized since they are too small and with consequently, greater biofilm biomass develop-
smooth. In addition, the colonization of microorganisms ment, as occurs in the wood [25].
is determined by particulate size and roughness [19−21].
In aquatic environments, sediments usually show a Living plants. Biofilms growing on living plants are
profile zonation in depth if they are sufficiently thick. In named epiphytic biofilms [17]. Submersed plants and
this sense, sediment thickness creates marked physical macroalgae living in wetlands and littoral zones are a
and chemical gradients that determine changes in the favorable habitat for microbial growth. Aquatic plants
sediment biofilm community. In this regard, surface present vast potential for microbial colonization and are
sediments support heterotrophic communities that frequently covered by a dense growth of algae, bacteria
include more opportunistic species. Bacterial density and other organisms favoring biofilm formation [21].
and activity are commonly higher in surface sediments However, in deeper parts of the plant, bacteria might be
and decrease with depth [9]. In rivers, the sediment favored due to light reduction produced by the host
hyporheic zone (interface between the river channel and plant, which affects algal development. Bacterial groups,
groundwater) offers protection against unfavorable con- Cytophaga-Flavobacteria-Bacteroidetes and Alpha-pro-
ditions to biofilm communities formed on sediments. teobacteria dominate epiphytic bacterial biofilms in
Also, grain size, sediment shape, and composition deter- marine and freshwater environments [26].
mine the porosity and hydraulic conductivity of the sedi- Plant and epiphytic biofilm interact in many ways,
ment, and influence most physical and chemical and the interaction may be both synergic and antagonistic.
processes [21]. The biofilm provides macrophytes with organic com-
pounds and carbon dioxide, and it also mediates nutri-
Dead plants materials. Dead plant materials (including ent uptake and enhances nutrient recycling [27]. In
wood and leaves) biofilm are named epixylic biofilm or addition, some bacterial species produce compounds
epixylon [17]. In this case, the substratum (i.e. dead against biofouling organisms while some other species
organic matter surfaces) presents both physical support enhance plant growth [28]. In return, plants provide a
medium for microbial colonization and organic matter substrate for biofilm formation and exude some gases
source for microbes. The relevance of the different organ- such as methane and different organic compounds from
isms forming epixylic biofilms is markedly different from the root zone, which are used by some biofilm bacteria.
other biofilm types. Different phyla of fungi are the prin- Consequently, different plant species, plant parts and
cipal microbial groups growing on dead plant material, environmental conditions may influence epiphytic bio-
mainly as a result of their lignocellulose degrading abil- films, determining microbial community composition
ity. However, bacteria, archaea, algae and metazoans and densities [26].
also form this kind of biofilms [22].
Different intrinsic and extrinsic factors influence the Suspended aggregates. Suspended aggregates made of
growth of microorganisms on dead plants materials. microorganisms, organic and inorganic particles are
Intrinsic factors refer to dead organic matter quality, highly fragile structures suspended in fresh and seawa-
such as cuticle toughness, nutrient content (particularly ter (usually after increased nutrients input) [29] and are
nitrogen and phosphorus), and the amount of less usually named lake snow, river snow or marine snow.
palatable substances such as lignin, or chemical inhibitors Marine snow consists of aggregates of diatoms, fila-
[23]. Environmental variables including water tempera- mentous cyanobacteria, bacteria, protozoans and diverse
ture, nutrient concentration or flow are extrinsic factors organisms with particles from the surrounding water,
[24]. Plant organic matter decomposition is determined glued together in a polymeric matrix released from phy-
by the effect of interaction between the plant material toplankton and bacteria. Anoxic conditions may exist
quality and the environmental variables. Additionally, within the snow particles so that diverse aerobic and

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 Multispecies Biofilms and Drinking Water Safety 477

anaerobic microbes colonize different niches [30]. Simi- and sediments) [30, 33]. First, the surface is conditioned
lar aggregates are formed in some water treatment sys- with a film of polysaccharides and proteins then, pioneer
tems, where they are called granules. planktonic cells attach to the surface, followed the pro-
Aggregation is a complex process (involving microbes) gressive arrival and biological adhesion of other
and is controlled mainly by particle density, size and microbes to form microcolonies until the mature biofilm
shape, settling velocity and the surface properties of the develops.
particle [31]. Furthermore, aggregates are affected by
the degree of porosity and the flux of both water and Species-to-Species Interactions in Biofilms
nutrient to and from microbial cells on the surface.
Quorum sensing (QS) that also refers to as intercellu-
Man-made surfaces. Diverse man-made surfaces lar signaling is a regulatory mechanism that plays a
including industrial and potable water system piping very significant role in the regulation of bacterial biofilm
can support biofilm formation, where biofouling may formation [34]. In different environments, biofilms fre-
occur by the deposition and growth of bacterial cells or quently exist as multispecies communities. The increase
flocs. In drinking water distribution systems Alpha- in the cell densities of such communities may result in
Beta- and Gamma-proteobacteria and Gram-positive high concentrations of QS signals in these communities.
bacteria are more dominant bacterial groups [32]. In This interaction is very important and highly valuable
marine environments, man-made structures, such as oil for the microbial strains producing the signals and those
and gas installations, aquaculture nets, and ship hulls, occupying the same habitat [34]. In recent times, the
can also provide surfaces for attachment. In this sense, importance of interspecies QS in shaping multispecies
the attachment of diatoms along with bacteria on man- communities has been of high growing interest. Fig. 1
made structures constitutes a major problem for artifi- outlines some major determinants for QS in multispecies
cial structures immersed in the marine environment [32, biofilms.
33].
The formation of attached microbial communities to Synergistic interactions. In natural environments, mul-
man-made surfaces follows similar sequential steps to tispecies biofilms exist as highly complex and dynamic
those observed for inert natural substrates (such as rock entities. The presence of some microbial species in such

Fig. 1. Communication in a natural multispecies biofilm. Biofilm communities are shaped by various interactions between micro-
bial species, including (1) competition between bacteria populations and their neighbours such as fungi (A), bacteria (B) and
microalgae (C), (2) quorum sensing derived from clonal growth in microcolonies (D) which may induce the protection against pro-
tozoa (E) and (3) interactions with second colonizers such as macroalgae spores (F) and invertebrate larvae (G).

December 2019 | Vol. 47 | No. 4

478 Reuben et al.

a multispecies community positively promotes and homoserine lactone QS molecule of P. aeruginosa, as

improves inter and intra-species communications as well well as bacteriocins produced readily inhibit L.
as the overall integrity of the formed biofilm. A typical pneumophila [40]. An and colleagues [41] reported that
example of synergistic interaction in the aquatic envi- in a dual-biofilm system between P. aeruginosa and
ronment is the occurrence of Legionella pneumophila Agrobacterium tumefacien, the former often dominate
(which is often a minority member) in multispecies the later during the growth of such biofilm by utilizing
biofilm in freshwater and other natural environments QS. Also, with the use of a QS molecule known as
[35]. Some bacterial species constituting the multispecies farnesol, yeast species appear to take a direct approach
biofilm readily promotes L. pneumophila survival and in tackling other microbial competitors within the multi-
persistence in such community [36]. Bacterial species species biofilm community. S. aureus shows enhanced
interestingly reported to provide synergistic interactions susceptibility to antibiotic as well as decreasing the
to the long term and continuous L. pneumophila per- formation of biofilm when exposed to farnesol [42].
sistence in multispecies biofilm include Pseudomonas Furthermore, in multispecies biofilm between yeast
fluorescens, P. putida, Flavobacterium sp., Klebsiella and other species (especially bacteria), yeast outsmarts
pneumonia and Empedobacter breve [36]. These bacteria other members of the biofilm through the usage of
produce matrix materials (mainly capsular and extra- farnesol, a QS molecule. The formation of biofilm
cellular) which promote adherence. Also, certain growth decreases with increased susceptibility to antibiotics
factors are provided by these bacterial species which when S. aureus is exposed to farnesol [42].
consequently stimulate the growth and viability of L. It has also been reported that through QS, matured
pneumophila in such a multispecies biofilm community bacterial biofilms can prevent eukaryotic predation [43].
[36]. Another classical example is the P. aeruginosa degrada-
Furthermore, synergistic interactions are often aug- tion of farnesol, the QS signal which is optimally needed
mented by the AI-2 QS in multispecies biofilms [37]. for the filamentation, maturation and biofilm formation
Dual bacterial species biofilms can also be formed even if by C. albicans. By utilizing virulence factors regulated
only one of the bacterial species in the biofilm produces by QS, P. aeruginosa can kill C. albicans [44].
AI-2 signal. This is of immense interest, depicting
species cooperation in multispecies biofilm communi- Listening but not talking. Some microbial species co-
ties. In the case of total inhibition and/or inactivation of habiting in a multispecies biofilm often respond to QS
AI-2 signals, mixed species biofilms become disrupted. signals produced by other species within the biofilm,
In another instance, some microbial phenotypes become thereby altering their physiology. The virulence factors
enhanced only in a multispecies biofilm [38]. Nevertheless, of P. aeruginosa become upregulated in the presence of
this majorly indicates the synergistic QS interactions AI-2, although P. aeruginosa does not produce AI-2. This
which can only be unraveled via in-depth molecular phenomenon may be of importance in multispecies
studies. environments such as cystic fibrosis (CF) airway
infections [45]. Similarly, bacteria in the ocean produce
Antagonistic interactions. Given the constant and fierce N-Acyl homoserine lactones (AHL) molecules which
competition for nutrients within multispecies biofilms in attract green seaweed’s (Ulva) [46]. Bacterial biofilms
a niche, certain mechanisms and products often regulate colonizing surfaces often initiate biofouling, before the
the survival of microbial species in such community. The secondary colonization by algae and other eukaryotic
most common mechanisms which augment competition organisms [47].
within microbial species in biofilm are the production of
bacteriocin (which is QS-regulated) and low pH [39]. P. QS signaling interference. Studies conducted lately
aeruginosa, Sphingomonas sp., Burkholderia cepacia, showed explicitly the capability of different organisms to
Acidovorax sp. and Aeromonas hydrophila inhibit L. degrade QS signals [34]. Once QS signals are degraded,
pneumophila once they exist in multispecies biofilm in their propagation within biofilm regions is prevented.
freshwater or other natural environments [36]. Basically, The degradation of QS signal may prevent signal propa-

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 Multispecies Biofilms and Drinking Water Safety 479

gation between regions forming biofilm in microbial S. gordonii colonizing the dental system as lately
communities existing in a spatially structured system. described in two different studies. The success of S.
This may further result in spatial confinement of the mutans in biofilm formation in such a multispecies
signal to different regions constituting the microbial system is usually inactivated by serine protease challisin,
community. which is secreted by S. gordonii, which interfere with a
AHL-lactonases and AHL-acylases are quorum QS signals (competence- stimulating peptide) responsible
quenchers very common in AHL systems [48]. While the for the formation of biofilm and subsequent colonization
hydrolyzation of the lactone ring is conducted by AHL- and plaque development [57]. Furthermore, of immense
lactonases, AHL-acylases hydrolyze amide linkages. interest within the oral cavity is the successful coloniza-
AHL-lactonases exist in several species of bacteria, tion by S. mutans in the presence of Actinomyces
although found foremost in Bacillus spp [49]. Only a few naelundii (also an early colonizer), with protease activity
bacteria including P. aeruginosa and Ralstonia spp. are [58]. Thus, jamming of QS may significantly control and
shown to produce AHL-acylases [50, 51]. influence waterborne pathogen biofilm formation, as
The success achieved by microbial species in interfer- well as disease outbreaks.
ing QS signaling is through the use of QS signal mimics
[52]. The inhibition of some strains of S. aureus QS by Factors Contributing to the Dynamics of
truncated peptides produced by some S. aureus agr QS Biofilm Composition in Water Distribu-
systems is a clear example of QS interference [53]. tion Systems
Another instance of bacterial QS inactivation by
eukaryotes was recently discovered in the Australian In DWDS, majority of microorganisms (95%) exist as
marine macroalga, Delisea pulchra, which disrupts P. biofilms [59]. The presence of biofilms attached to the
aeruginosa AHL signaling. Thus, hindering biofilm water supplies pipe inner surface in the DWDS serve as
formation on leaves surfaces by microorganisms [54]. a major source for the high microbial population. This is
of great public health significance as it affects the quality
Jamming of QS in multispecies biofilms. Although wide and wholesomeness of drinking water. Despite the diver-
range of functions, including the control of virulence sities of the conditions (nutritional and physicochemical)
traits and bacterial biofilm are regulated by QS, and An in DWDS, biofilms evolved mechanisms to successfully
and others [41] noted that the development of mixed survive and flourish [60]. Increased water turbidity,
species populations is also actively carried out by odor, taste, reduction in water flow as a result of reduced
QS. As earlier stated above, QS interference, inhibi- pressure, corrosion and most importantly distribution of
tion and impairment can be carried out by individual pathogens are the various problems associated with bio-
bacterial species involved in biofilm. Also, QS films formed by multiple microbial species in DWDS. E.
molecules can be degraded by certain enzymes pro- coli, Helicobacter pylori, Salmonella spp. and a host of
duced by bacteria [48]. The formation of biofilm by bacte- other human pathogens and various microbial toxins
ria is directly affected by QS interferences within such detrimental to humans are often trapped by multispecies
community. A typical example is the inability of V. biofilms in DWDS [61]. The presence of different groups
cholerae to form biofilm in the presence of AiiA, an AHL of microbes including viruses, bacteria algae, protozoans
lactonase, produced by Bacillus cereus [55]. Also, the and bacteria forming a mixed microbial community in
formation of biofilm by P. aeruginosa is often inhibited the form of biofilm is of grave concern. Attention should
through interference with P. aeruginosa PAO1 QS in be given to such relationships, molecular mechanisms
the presence of amines (aliphatic) and phenolic groups involved and products formed in order to elucidate and
from other bacteria [56]. control is effects on DWDS.
Bacterial communication signals and degrading Once a negligible number of bacteria succeeds in
enzymes can be found in the oral cavity. The coloniza- accessing the water distribution system, they multiply
tion by S. mutans depends proportionately on their spontaneously especially when environmental and
interactions with other early microbial species, such as nutritional conditions become favorable [62]. Biofilms

December 2019 | Vol. 47 | No. 4

480 Reuben et al.

formed in DWDS are influenced by the factors which and these bacterial over the years have gradually
include physicochemical conditions of the water, microbial evolved resistance mechanisms against its effect [64].
resistance to disinfection, availability of nutrients, and Biofilm attachment (which often protects microbial cells)
types and materials of piping systems [63]. on surfaces in distribution system, microbial cells aggre-
gation, cell spore formation among others are also
Water source. The origin and source of water used in factors contributing to increased bacterial resistance to
distribution systems have major influence on microbial disinfectants [67].
communities. Several studies extensively reported the
effects of water source on the composition microbial com- Availability of nutrients. In the presence of nutrients
munity [63]. Furthermore, it was also reported that a microbial growth blossom and the biofilm formation
clear distinction in the diversities and profiles of micro- become enhanced. Microbial stability on distribution
bial community exist among different DWDSs. With the systems is usually affected by the quantity of nutrients,
application of multivariate analysis of surface and most especially organic carbon which supports microbial
groundwater, bacterial communities can be clearly dis- regrowth [60]. With regards to the nature and type of
tinguished from in DWDS. Nevertheless, recent studies disinfectant used, assimilable organic carbon (AOC)
indicated that flowing water is the major source of bacte- presence can favor rapid bacterial regrowth in DWDS.
ria in DWDS [62]. There is a significant relationship between bacterial
ability to form biofilm and AOC uptake. Furthermore,
Ineffective disinfectants. The application of disinfec- once AOC becomes reduced in the distribution systems,
tants during water treatment has a direct influence on bacterial ability to form biofilm declines [66].
both microbial population and their diversity [63].
Besides the fact that disinfectants eliminate microbes Plumbing and piping materials. In DWDSs, metallic,
once administered appropriately, they also facilitate the plastic and cementitious pipes are generally used. The
formation of certain substances which are easily biode- quality of water in distribution system is directly related
gradable by microbes. These biodegradable substances to the type of material used in such a system [68]. Once a
(usually organic) further enhance the formation of biofilms, material is capable of supplying nutrients and enriching
as these microbes utilize them as their major energy microbial growth, the formation of biofilm will be greatly
source [65]. Although bacterial population can rapidly facilitated. Most developed countries screens piping
decline on the application of appropriate concentration material to ascertain that they influence drinking water
of chlorine during water treatment, Gibbs and colleagues quality, most especially microbial growth enhancers. In
[64] observed bacterial regrowth as the chlorine concen- DWDS, it has been reported that high bacterial densities
tration decreases. Some disinfectants potency rapidly (109 bacteria·cm-2) exist in biofilms within pipe surfaces
fades out before the dead-end of distribution systems [69]. It has also been documented that microbes deterio-
thereby favoring massive regrowth of microbial cells. rate concrete piping in distribution systems [64]. Such
deterioration is often complex and requires different
Bacterial resistance to disinfectants. Findings by different microbial groups.
authors lately revealed the high number of bacterial
multiplication and survival in culturable quantities in Temperature and season. Increase or decrease in tem-
the presence of appropriate concentrations of disinfectants. perature influences microbial growth in the DWDS [61].
The presence of these bacteria depicts their resistance to Temperature varies alongside seasons, with both
disinfectants [66]. Presently, research on the roots and influence microbial growth hence biofilm formation in
causes of bacterial resistance to chlorine in the United distribution systems. Whereas some authors reported
Kingdom and parts of Asia have commenced in earnest. seasonal differences in microbial community within the
Bacterial resistance to chlorine, been one of the most DWDS [70], others opined that microbial communities
widely used disinfectants should not be a surprise. This are not affected by the change in seasons [63], hence
is because most distribution systems only apply chlorine biofilm formation.

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 Multispecies Biofilms and Drinking Water Safety 481

Contribution of Biofilms in Disease Trans- are sheltered from adverse environmental factors capa-
mission via Water Distribution Systems ble of inhibiting or destroying them. This is also applica-
ble to pathogens protected by biofilms in humans and
It has been earlier stated that the source of water other animals, which consequently evade the immune
directly determines the kind of microbial composition system of their host and also withstand the effects of
and interaction within water distribution systems. Bio- antibiotics [73].
films formation congregates different groups of microbial In recent times, large water bodies, especially oceans
species which enables them to interact freely [62]. Many are increasingly been discovered to be major pathogen
pathogens including Aeromonas spp, Klebsiella spp, sources [75]. These water bodies accommodate different
Pseudomonas spp, Enterobacter spp amongst others biofilm-forming pathogens which become integral
have reportedly been isolated from biofilms in distribu- members of such an environment. Fong and colleagues
tion systems containing both disinfected and non-disin- [73] gave an extensive description of the relationship
fected water [67]. Of immense public health interest is existing between V. cholerae biofilm and cholera trans-
the increase in planktonic bacterial population as a mission and outbreaks. To fully unravel the role of bio-
result of regrowth from biofilms or raw water source. films in disease transmission, it is necessary to
Although drinking water quality is microbiological understand the molecular mechanisms of biofilm forma-
assessed based on indicators (coliforms) presence, it is tion by bacteria.
important that heterotrophic bacterial population Environmental biofilms produced by pathogens are
should also be controlled as many have successfully capable of transmitting such pathogens to different com-
become opportunistic pathogens causing serious infec- munities, thereby initiating disease outbreaks [74]. A
tions in humans [71, 72]. typical example of this phenomenon has been shown in
Several emerging and re-emerging human pathogens Bangladesh, being an endemic area for cholera. Toxigenic
such as Yersinia enterocolitica, Campylobacter spp, V. cholerae were isolated from biofilms in surface water.
enterotoxigenic E. coli, Helicobacter pylori, Salmonella Furthermore, sufficient quantity of V. cholerae cells
Typhimurium and also Cryptosporidium parvum have existing as biofilms in cholera patients are capable of
reportedly survived in biofilms in water distribution initiating infections once shedded [75−77]. As such, V.
systems [73]. Multispecies biofilms involving cells of cholerae biofilms have vital role in both the survival and
bacteria and cysts of protozoans, yeast cells and other distribution of V. cholera. Most importantly, other
species of fungi and algae can harbor and provide a pathogens associated with water are capable of exhibit-
favorable environment for the survival and proliferation ing similar patterns in their ecology and also the epide-
of pathogens. These pathogens can subsequently detach miology of diseases they cause.
into water flow in the distribution systems. The results of our previous study further indicated the
In most cases, the public health significance of biofilm capability of V. cholera to form biofilms on plexiglass
is salient and indirect. It is glaring that biofilms can discs, which are abiotic surfaces in Bangladesh aquatic
weaken the pipe integrity through corrosion and also environment. The biofilms were also observed to provide
compromise the use of coliforms as indicators. Aesthetic V. cholerae with a microenvironment in which rugose
problems may not pose a direct health risk to the public variants can persist [13].
but are clear indicators of biofilm presence and flaws in Colonized with V. cholera in the form of biofilms
the system which may affect the public. particulates and planktons in the seawater of the Bay
of Bengal further introduces cholera bacteria into the
Role of biofilms in disease transmission and water surrounding brackish ecosystems in Bangladesh. Major
quality. Bacterial adhesion to solid surfaces and their serogroups of V. cholera (including O1 and O139) living
eventual formation of biofilms have a major impact on in biofilms have been isolated in all seasons throughout
disease transmission and persistence [74]. Once biofilms the year, responsible for the endemic nature of cholera in
are formed in the aquatic and other natural environ- that entire region [18, 78]. Some serotypes of V. cholera
ments, different pathogens become residential as they exist in nonculturable state thrive far better in aquatic

December 2019 | Vol. 47 | No. 4

482 Reuben et al.

environment than when shed in stools of cholera shown that the formation of microcolony and the produc-
patients [18], which are later washed back to the aquatic tion of QS induced inhibitors by bacterial biofilms are
environment. able to resist protozoan grazing [10] Fig. 2.
Apart from the above-stated mechanisms developed
Protozoan grazing of aquatic biofilms: reservoirs of by bacterial biofilms against protozoan predation, it has
pathogenic bacteria. In a microbial food chain, bacteria been recently discovered that extensive biofilm forma-
within the natural environment become food for other tion arising as a result of the cooperation involving dif-
living organisms including protozoa. This eventually ferent species of bacteria can also resist predation [79].
depletes the number of bacteria within such habitats. Also, certain unknown toxin produced by V. cholera bio-
Nevertheless, bacteria have developed diverse strategies films as induced by QS has been reported to greatly
against protozoa predation. The formation of biofilms is resist grazing most especially in fully matured biofilms
one of the most effective ways to avoid protozoan graz- [80]. In the aquatic environment, heterotrophic flagel-
ing. Also, bacteria develop other strategies against pro- lates stimulate biofilm formation as individual bacterial
tozoan predation; various changes in the bacterial cells greatly reduced [78]. Furthermore, it has been
physiology and morphological changes like decreased reported that protozoan non-selective grazing and
biomass [79]. release of nutrients cause stimulation which results in
The ability of protozoa to fully colonize bacterial bio- the overwhelming domination by fast-growing bacteria,
films in the environment occurs in three stages. Hetero- thereby outgrowing their predators. The inability of
trophic flagellates are often the first to colonize surfaces mobility makes biofilms unable to escape protozoan
immediately after exposure as a result of their mobility grazing which unduly increases the intensity of grazing
and high population, after which ciliates and amoebae. pressure. The abundance of bacterial biofilms in diverse
The success associated with grazing relies basically on environments is an indication of high anti-predator and
the grazer’s mode of nutrition as well as the bacterial increased fitness with immense mechanisms for grazing
biofilm developmental stage [77, 79]. Clearly, in contrast resistance long evolved as a result of close ecological
to planktonic cells, protozoa encounter a different feed- associations between bacteria and protozoa.
ing environment once biofilms are formed. As previously Certain flagellates act as bacterivores in the aquatic
reported, there is 1.75 higher levels of biofilm metabo- environment, thereby affecting the spontaneous devel-
lism when ciliate grazers are introduced to biofilms opment of biofilm via sloughing and fragmentation. This
formed by the yeast-Cryptococcus spp when compared further alters the distribution of EPS and other individ-
with non-grazing controls. The preference for the matrix ual biochemical constituents of biofilms, reducing the
of bacterial biofilms as against individual biofilm cells chances of multispecies biofilm formation. Some protozoa
depicts EPS as nutrient source for protist. Studies have such as Acanthamoeba castellanii and Colpoda maupasi

Fig. 2. The effects of flagellate Rhynchomonas nasuta grazing on Pseudomonas aeruginosa biofilms. (A) Three-day-old biofilms
of P. aeruginosa PAO1 growing without flagellate. (B) Three-day-old biofilms of P. aeruginosa PAO1 growing with flagellate. (C)
Seven-day-old biofilms of P. aeruginosa PAO1. Biofilms were regrown for 3 days before the addition of flagellate. Scale bar = 50 μm
[14, 150].

http://dx.doi.org/10.4014/mbl.1907.07007
 Multispecies Biofilms and Drinking Water Safety 483

thrive predominantly as biofilm grazer. They become for microbial community modeling, it becomes necessary
integrated into biofilm thereby reducing the thickness of to fully ascertain the mechanisms underlying microbial
biofilm by up to 60% [70, 79]. Queck and others [43] ecology of multispecies biofilms in the aquatic environ-
showed that protozoan predation using different modes ment. Physiological and morphological heterogeneity
of feeding and motility gave rise to different structures of coupled with both intrinsic and extrinsic interrelations
multispecies biofilms morphology. Of beneficial to make environmental biofilms much more complex enti-
bacteria is the increase mass transfer of nutrient into ties. Further studies concentrating on the antagonistic
biofilms as a result of protozoan grazing, thus accelera- interactions in multispecies biofilm in the aquatic envi-
tion microbial growth [80]. ronment will provide clues on improving water quality
Bacteria living in a biofilm can change their response and safety. Furthermore, the use of promising molecular
to protozoa, thereby using such protozoa as pathogens technologies will fully unravel the detailed interactions
reservoir. Amoebae harbor Listeria spp, Mycobacterium between biofilms in aquatic environment and the operat-
spp. and several other pathogens which can subse- ing ecological processes, thus aiding in managing multi-
quently be released to the environment. Unique and species biofilms to provide services to society.
more invasive forms of pathogens with biochemical and
morphological changes result from protozoa involved in Acknowledgments
biofilm grazing than those cultured in vitro [80]. It is
now obvious that protozoa within the environment This research has been financed by the Bangladesh Academy of
involved fully in the distribution and maintenance of Science under BAS-USDA program code no. LSC 33

pathogens. More studies will further reveal the molecu-

lar mechanisms involved in protozoan grazing, biofilm Conflict of Interest
resistance and pathogen persistence in the environment.
The authors have no financial conflicts of interest to declare.

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