Protozoan impact on bacterial biofilm formation

Rychert, Krzysztof; Neu, Thomas R.

doi:10.2478/v10120-009-0017-x

Cited by 8 publications

(6 citation statements)

References 19 publications

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“…Protozoa have also been demonstrated to excrete growth stimulating products which could potentially induce flocculation [ 48 ]. For example, the co-incubation of activated sludge bacteria with sludge protozoa composed of attached, crawling ciliates, flagellates and amoeba for 48 h, resulted in biofilms that had 2000% more biomass than the biofilms that were not exposed to protozoan predation [ 11 ]. In addition, polymeric substances such as extrusomes, cellular debris and undigested residues secreted from protozoa could also facilitate aggregation between bacterial flocs [ 49 ].…”

Section: Discussionmentioning

confidence: 99%

Microbial predation accelerates granulation and modulates microbial community composition

et al. 2021

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Background Bacterial communities are responsible for biological nutrient removal and flocculation in engineered systems such as activated floccular sludge. Predators such as bacteriophage and protozoa exert significant predation pressure and cause bacterial mortality within these communities. However, the roles of bacteriophage and protozoan predation in impacting granulation process remain limited. Recent studies hypothesised that protozoa, particularly sessile ciliates, could have an important role in granulation as these ciliates were often observed in high abundance on surfaces of granules. Bacteriophages were hypothesized to contribute to granular stability through bacteriophage-mediated extracellular DNA release by lysing bacterial cells. This current study investigated the bacteriophage and protozoan communities throughout the granulation process. In addition, the importance of protozoan predation during granulation was also determined through chemical killing of protozoa in the floccular sludge. Results Four independent bioreactors seeded with activated floccular sludge were operated for aerobic granulation for 11 weeks. Changes in the phage, protozoa and bacterial communities were characterized throughout the granulation process. The filamentous phage, Inoviridae, increased in abundance at the initiation phase of granulation. However, the abundance shifted towards lytic phages during the maturation phase. In contrast, the abundance and diversity of protozoa decreased initially, possibly due to the reduction in settling time and subsequent washout. Upon the formation of granules, ciliated protozoa from the class Oligohymenophorea were the dominant group of protozoa based on metacommunity analysis. These protozoa had a strong, positive-correlation with the initial formation of compact aggregates prior to granule development. Furthermore, chemical inhibition of these ciliates in the floccular sludge delayed the initiation of granule formation. Analysis of the bacterial communities in the thiram treated sludge demonstrated that the recovery of ‘Candidatus Accumulibacter’ was positively correlated with the formation of compact aggregates and granules. Conclusion Predation by bacteriophage and protozoa were positively correlated with the formation of aerobic granules. Increases in Inoviridae abundance suggested that filamentous phages may promote the structural formation of granules. Initiation of granules formation was delayed due to an absence of protozoa after chemical treatment. The presence of ‘Candidatus Accumulibacter’ was necessary for the formation of granules in the absence of protozoa.

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Section: Discussionmentioning

confidence: 99%

Microbial predation accelerates granulation and modulates microbial community composition

et al. 2021

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“…In the mixed-species consortia there was an increase by ∼2.5-fold in total bacterial cell numbers (all four species combined) in the grazed biofilm compared to the non-grazed biofilm, whereas in the planktonic fractions grazing reduced total cell numbers by ∼1.8-fold, emphasizing the protective nature of the biofilm mode of life. Evidence that grazing pressure is positively correlated with the formation of cell clusters has come from both monospecies laboratory biofilm ( Matz et al, 2004 , 2005 ) and from natural/semi-natural multispecies biofilm ( Wey et al, 2008 ; Rychert and Neu, 2010 ; Corno et al, 2015 ). Grazing induced biofilm formation could reflect either an active defense mechanism ( Matz and Kjelleberg, 2005 ; Friman and Buckling, 2014 ) or a passive mechanical process where the movement of the protozoan cells drives the bacterial cells to the substratum ( Wey et al, 2012 ).…”

Section: Discussionmentioning

confidence: 99%

Synergistic Interactions within a Multispecies Biofilm Enhance Individual Species Protection against Grazing by a Pelagic Protozoan

et al. 2018

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Biofilm formation has been shown to confer protection against grazing, but little information is available on the effect of grazing on biofilm formation and protection in multispecies consortia. With most biofilms in nature being composed of multiple bacterial species, the interactions and dynamics of a multispecies bacterial biofilm subject to grazing by a pelagic protozoan predator were investigated. To this end, a mono and multispecies biofilms of four bacterial soil isolates, namely Xanthomonas retroflexus, Stenotrophomonas rhizophila, Microbacterium oxydans and Paenibacillus amylolyticus, were constructed and subjected to grazing by the ciliate Tetrahymena pyriformis. In monocultures, grazing strongly reduced planktonic cell numbers in P. amylolyticus and S. rhizophila and also X. retroflexus. At the same time, cell numbers in the underlying biofilms increased in S. rhizophila and X. retroflexus, but not in P. amylolyticus. This may be due to the fact that while grazing enhanced biofilm formation in the former two species, no biofilm was formed by P. amylolyticus in monoculture, either with or without grazing. In four-species biofilms, biofilm formation was higher than in the best monoculture, a strong biodiversity effect that was even more pronounced in the presence of grazing. While cell numbers of X. retroflexus, S. rhizophila, and P. amylolyticus in the planktonic fraction were greatly reduced in the presence of grazers, cell numbers of all three species strongly increased in the biofilm. Our results show that synergistic interactions between the four-species were important to induce biofilm formation, and suggest that bacterial members that produce more biofilm when exposed to the grazer not only protect themselves but also supported other members which are sensitive to grazing, thereby providing a “shared grazing protection” within the four-species biofilm model. Hence, complex interactions shape the dynamics of the biofilm and enhance overall community fitness under stressful conditions such as grazing. These emerging inter- and intra-species interactions could play a vital role in biofilm dynamics in natural environments like soil or aquatic systems.

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“…Furthermore, the addition of AHLs to the SBR markedly increased the production of EPS, which mediates contact between bacterial cells [8,9]. Other biological factors such as predation have been demonstrated to enhance bio lm formation for several bacterial species [10][11][12]. Predation on those free-living bacteria may therefore represent a strong pressure selecting for bacteria that are tightly embedded in aggregates of biomass.…”

Section: Introductionmentioning

confidence: 99%

Microbial Predation Accelerates Granulation and Modulates Microbial Community Composition

Chan

Ismail

Tan

et al. 2021

Preprint

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BackgroundBacterial communities are responsible for biological nutrient removal and flocculation in engineered systems such as activated floccular sludge. Predators such as bacteriophage and protozoa exert significant predation pressure and cause bacterial mortality within these communities. However, the roles of bacteriophage and protozoan predation in impacting granulation process remain limited. Recent studies hypothesised that protozoa, particularly sessile ciliates, could have an important role in granulation as these ciliates were often observed in high abundance on surfaces of granules. Bacteriophages were hypothesized to contribute to granular stability through bacteriophage-mediated extracellular DNA release by lysing bacterial cells. This current study investigated the bacteriophage and protozoan communities throughout the granulation process. In addition, the importance of protozoan predation during granulation was also determined through chemical killing of protozoa in the floccular sludge.ResultsFour independent bioreactors seeded with activated floccular sludge were operated for aerobic granulation for 11 weeks. Changes in the phage, protozoa and bacterial communities were characterized throughout the granulation process. The filamentous phage, Inoviridae, increased in abundance at the initiation phase of granulation. However, the abundance shifted towards lytic phages during the maturation phase. In contrast, the abundance and diversity of protozoa decreased initially, possibly due to the reduction in settling time and subsequent washout. Upon the formation of granules, ciliated protozoa from the class Oligohymenophorea were the dominant group of protozoa based on metacommunity analysis. These protozoa had a strong, positive-correlation with the initial formation of compact aggregates prior to granule development. Furthermore, chemical inhibition of these ciliates in the floccular sludge delayed the initiation of granule formation. Analysis of the bacterial communities in the thiram treated sludge demonstrated that the recovery of ‘Candidatus Accmulibacter’ was positively correlated with the formation of compact aggregates and granules.ConclusionPredation by bacteriophage and protozoa were positively correlated with the formation of aerobic granules. Increases in Inoviridae abundance suggested that filamentous phages may promote the structural formation of granules. Initiation of granules formation was delayed due to an absence of protozoa after chemical treatment. The presence of Candidatus Accumulibacter was necessary for the formation of granules in the absence of protozoa.

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Protozoan impact on bacterial biofilm formation

Cited by 8 publications

References 19 publications

Microbial predation accelerates granulation and modulates microbial community composition

Microbial predation accelerates granulation and modulates microbial community composition

Synergistic Interactions within a Multispecies Biofilm Enhance Individual Species Protection against Grazing by a Pelagic Protozoan

Microbial Predation Accelerates Granulation and Modulates Microbial Community Composition

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