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Multiple micro-predators controlling bacterial communities in the environment
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ScienceDirect Multiple micro-predators controlling bacterial communities in the environment Julia Johnke1, Yossi Cohen2, Marina de Leeuw3, Ariel Kushmaro3, Edouard Jurkevitch2 and Antonis Chatzinotas1 Predator–prey interactions are a main issue in ecological theory, including multispecies predator–prey relationships and intraguild predation. This knowledge is mainly based on the study of plants and animals, while its relevance for microorganisms is not well understood. The three key groups of micro-predators include protists, predatory bacteria and bacteriophages. They greatly differ in size, in prey specificity, in hunting strategies and in the resulting population dynamics. Yet, their potential to jointly control bacterial populations and reducing biomass in complex environments such as wastewater treatment plants is vast. Here, we present relevant ecological concepts and recent findings on micropredators, and propose that an integrative approach to predation at the microscale should be developed enabling the exploitation of this potential. Addresses 1 Department of Environmental Microbiology, Helmholtz Centre for Environmental Research - UFZ, 04318 Leipzig, Germany 2 Department of Plant Pathology and Microbiology, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, 76100 Rehovot, Israel 3 Department of Biotechnology Engineering and The National Institute for Biotechnology, Ben Gurion University, 84105 Beer Sheva, Israel Corresponding author: Jurkevitch, Edouard ([email protected])
Current Opinion in Biotechnology 2014, 27:185–190 This review comes from a themed issue on Environmental biotechnology Edited by Hauke Harms and Howard Junca
0958-1669/$ – see front matter, # 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.copbio.2014.02.003
Introduction Predation is a major mode of interaction between organisms in the living world, with predators spanning from the submicron level (bacteriophages) to meters in size [1]. Predation in macro-organisms has been the subject of many studies but our understanding of its importance at the microscale is lacking. Microbes constitute the largest biomass of organisms on Earth. Accordingly, the microbial food web has been shown to be a main driver of the planet’s biogeochemical cycles, controlling nutrient recycling and trophic transfer of the major six elements H, C, www.sciencedirect.com
N, O, S and P [2]. Although predatory interactions between microbes appear to be the largest factor of bacterial mortality in many ecosystems [3,4], there is still a considerable gap of knowledge on the processes they affect, and of their dynamics at the microscale. Filling this gap requires bringing together classical ecological theory and the understandings of the particulars of organisms at this scale. Consequently, questions resulting from predator–prey interactions such as the role of multispecies predator– prey systems [5] or more recently the question, how diversity affects ecological processes [6], that is, the relation between biodiversity and ecosystem function (BEF) should be addressed in this context. A recent meta-analysis has revealed a general positive mean predator (secondary consumers) richness effect on prey suppression, though species identity seems to contribute substantially to the variability observed in experiments [7]. Niche complementarity, overexploitation of prey, reduction in prey species richness and consequently reduced prey production, or dominance by less competitive prey species are potential mechanisms by which increasing predator diversity can decrease total prey biomass [8]. Differences in prey use patterns can produce saturating (i.e. maximum redundancy), additive (i.e. maximum complementarity) or mixed effects [9], whereas antagonistic interactions may negatively affect consumption rates of prey [10]. Particularly, the prey range of a predator (i.e. generalist or specialist) may largely determine the importance of top-down control as compared to a resource driven bottom-up control of the prey [11]. An important aspect in the context of multiple predation is to know whether or not intraguild predation (IGP) occurs in a given habitat. IGP combines aspects of predation and competition and refers to predation among two predator species which also compete for the same prey [12,13]. Such negative interactions strongly impact predator-diversity effects and eventually result in lowered prey suppression rates; moreover IGP effects vary across different ecosystems [12], while densities of alternative prey resources may affect the strength of IGP [14]. Likewise, it is equally important to address the role of prey species diversity on the strength of top-down control. Several potential mechanisms have been proposed so far: predation-resistant or inedible species can dominate Current Opinion in Biotechnology 2014, 27:185–190
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mixed assemblages, while diverse resources can reduce the efficiency of specialist consumers or provide a more complete range of nutritional resources, resulting in higher consumer biomass and top-down control [8,15,16]. Similarly, the production of toxic substances by a cooperating bacterial community can protect neighboring, non-toxic bacteria from predation. This may facilitate the establishment of predation-sensitive bacteria and may lead to an increased bacterial diversity [17].
Predatory key players at the microscale At the microscale, three key players convey these interactions: eukaryotic protists, predatory bacteria and bacteriophages. Protists are ubiquitous and overall generalist grazers of prokaryotes in marine, aquatic and terrestrial ecosystems. They represent one of the major factors accounting for the mortality of prokaryotes in the environment [2] greatly affecting microbial nutrient recycling and regeneration. A key aspect of this predatory interaction is the removal of a high number of bacteria in a short amount of time. In laboratory settings soil protists require between 129 and 12,000 bacteria per cell division [18]. The protistan community in natural ecosystems follows a successional pattern depending on the nature of the grazer. For example, early biofilm colonizers (or generalists, including flagellates and ciliates) are highly mobile, allowing fast surface feeding, while intermediate late colonizers (some ciliates and amoebas) are classified as specialists and are abundant in mature biofilms [19]. Protists further differ in feeding strategies by showing prey preferences (depending on bacterial size, motility, shape, cell surface characteristics and food quality [20,21]), which is one explanation, why different bacterivorous protists coexist in the same habitat. Molecular environmental surveys have revealed that protistan communities are much more diverse than previously assumed [22]. Even closely related and morphologically similar strains show high functional diversity and have different impact on prey communities [23]. Although experimental manipulation of protistan grazing pressure was found to induce shifts in bacterial community structure [21], direct analyses of predatory protist–prey interactions are still rare. With the development of new tools enabling, for example, the tracking of stable isotopelabeled prey cells [24,25] we can hopefully gain new insights in the future. Consistent with the keystone predation model, predation resistant and vulnerable species coexist at intermediate productivities [26]; negative selection effects at higher productivity lead to a stronger selection of predation resistant, albeit unproductive species [27], and thus a decline in prey diversity. The diet breadth of a predator (generalist vs. specialist) can also change the relative strength of bottom-up and top-down forces in bacterial communities, though current data probably do not allow a Current Opinion in Biotechnology 2014, 27:185–190
generalization [28]. Moreover, increasing protist species richness may result in an increase in prey evenness, probably due to the reduction of competitive interactions and the growth of subdominant species in diverse bacterial systems [29]. In accordance with current ecological theories, prey resources are more substantially reduced when exposed to a diverse set of protists with different feeding modes [29], pointing to complementarity effects in multi-predator assemblages [30]. Recent evidence that presence of an intraguild prey may even induce trophic polymorphisms of freshwater ciliates, points to a phenotypic plasticity that allows organisms to adapt to changes in the environment, with consequences for the diet breath and the community dynamics [31]. Bacteriophages (phages) in aquatic ecosystems can reach densities 10–100 times higher than bacteria [4], with viral lysis being responsible for up to 71% of bacterial mortality [32]. As opposed to protists, phages are mostly highly host-specific, a characteristic that may lead to oscillations in both predator and prey as suggested by the ‘killing the winner’ hypothesis: bacterial populations are affected in a density dependent manner so that the most abundant bacteria are preferentially targeted [33], thereby maintaining microbial diversity [34]. Another hypothesis, antagonistic coevolution claims that bacterial strains develop resistance to bacteriophages attacking them [35], leading to an arms-race [36,37]. Indeed, Pal et al. [38] showed that bacteria with high mutation rates are selected in the presence of bacteriophages. Rapid mutations in both populations may also lead to oscillatory dynamics in microbial populations. Yet, more complex bacteriophage-driven effects may be at play as bacterial killing may also contribute nutrients through the release of prey breakdown products, bringing about bacterial growth [39]. Bacteriophages can also act as defense agents for bacteria under protist predation pressure [40]. For instance, the phage-encoded Shiga toxin (Stx) negatively impacted a Tetrahymena thermophila population in a lab experiment. Bacteria containing the toxin-encoding phage showed a survival advantage over bacteria that were not infected. A similar mechanism was observed for Acanthamoeba in coculture with phage-infected Corynebacterium diphteriae. Here, intoxication only occurred when the exotoxin was released after the internalization of the bacteria by the amoeba. Therefore, bacteria can use phages to function as ‘Trojan horse’ in order to survive protist attacks (dotted lines in Figure 2). Predatory bacteria include obligate as well as facultative predators. The former are constituted of several genera collectively known as the Bdellovibrio and like organisms (BALOs), which prey on many Gram negative bacteria, and are ubiquitously distributed in terrestrial and aquatic environments [41]. BALOs are periplasmic (i.e. they www.sciencedirect.com
Bioactive fungal polysaccharides Johnke et al. 187
penetrate, grow and divide within the prey [42]) or epibiotic (they attach to the cell wall, and grow and divide outside the prey [41]) (Figure 1). By contrast to the generalist nature of protist predation, and the specific interactions of phages with their hosts, BALOs are neither true generalist nor hard-core specialists [43]. Instead, prey range differs between isolates, being more or less broad. Consequently, the overall breath of BALO prey is unknown and the impact of BALOs on bacterial communities not defined. Experimental manipulations of BALO prey interactions have shown that the addition of a specific prey into natural samples leads to specific responses in BALO populations [43], more complex than the ‘killing the winner’ patterns observed in wastewater phages [34]. Furthermore, Shemesh et al. [44] showed that BALOs do not eradicate prey from cultures as prey populations exhibit phenotypic plasticity leading to increased resistance to predation, and Gallet et al. [45,46] demonstrated that BALOs and prey rapidly evolve to yield populations varying in predatory and resistance capabilities, respectively. Although ubiquitous, BALOs are only one component of the ill-defined bacterial predatory community. Recent genome-based studies have shown that specific molecular signatures are found in predatory bacteria, opening the way for a better classification of predatory activity in ecosystems and the uncovering of novel predators [47].
Perspectives of integrated micro-predation research In WWTPs heterotrophic communities efficiently remove organics, nutrients, toxic substances, and pathogens. The very nature of micro-predation can potentially improve wastewater treatment by specifically removing bacterial pathogens (by BALOs and phages) or by reducing the
overall bacterial load (by BALOs and protists). As an example, protists can filter as much as 1000 nl/h, implying that the entire liquid of an activated sludge plant can be filtered in less than 1 h [48]. Yet, crucially assessing phenomena such as prey preferences, environmental effects, and IGP, in relation to a system’s productivity, constitute crucial goals for a reliable application in biotechnological settings such as WWTP [49]. Most interactions between the here presented micro-predator groups remain understudied [60,62,64]; even more importantly, their combined effects on bacterial communities are unknown (Figure 2). Network analyses have recently been shown to allow untangling interactions and co-occurrence patterns within complex microbial communities and revealing environmental conditions that correlate with these relationships [50]. So far, by contrast to protist [48], few studies on waste water treatment processes have included phages or BALOs [51]. Bacteriophages have been widely searched for and detected in WWTP [34,52] because of their capacity to affect the bacterial community [34]. This was shown in the dewatering of sludge which is improved by using phages to degrade the bacterially produced exopolysaccharide, aiding floc formation [53,61]. Furthermore, phages can be used to reduce excess biological sludge and excess foaming [55]. Using Fluorescence in Situ Hybridization (FISH) on waste water sludge flocks samples, Dolinsek et al. [51] demonstrated interactions of the BALO Micavibrio with the nitrite-oxidizing bacteria, sub-lineage I Nitrospira cluster. Although only about 4% of the sub-lineage I Nitrospira aggregates were surrounded by Micavibrio-like bacteria, it was posited that the predators may prevent any particular nitrifier strain from becoming dominant, thus driving diversification,
Figure 1
500nm
1 µm
1 µm
Current Opinion in Biotechnology
Bdellovibrio bacteriovorus (a periplasmic predator) within an Escherichia coli prey (left); Bdellovibrio exovorus (an epibiotic predator) attached to a Caulobacter crescentus prey (right). www.sciencedirect.com
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References and recommended reading
Figure 2
Papers of particular interest, published within the period of review, have been highlighted as:
IGP
of special interest of outstanding interest
Protists
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Possible interactions among protists, BALOs and phages in multipredator communities. Although some of the pictured interactions have been described already, others are severely understudied (dashed lines). Protists have been shown in a few cases to affect virus (phage) populations either indirectly by feeding on infected bacteria (coincidental IGP [57]) or by direct grazing on virus-like particles (omnivorous IGP [58]). Vice versa, viruses are likely to infect heterotrophic protists with yet unclear consequences for top-down control of bacteria [59] or use bacteria as ‘Trojan horse’ in order to kill protists (dotted line) [40]. BALOs, like other bacteria, can be infected with phages [63,65], while any direct interaction with protists is unknown. All of the three micropredators graze on bacteria, though, with different prey range from highly specific (phages) up to rather unspecific predation (protists) as indicated by the thickness of the arrows.
increasing resistance to perturbations and the stability of nitrification in engineered and natural ecosystems [51].
Conclusions We believe that development of biologically realistic models of trophic interactions in diverse systems and subsequently appropriate management strategies (as in WWTPs) will require the unification of research on BEF, functional traits, predator and prey habitats, and how these interact with environmental heterogeneity and complexity [54]. Several predator and prey traits including microhabitat use, mobility and patchy distribution, feeding niches and behavior have only insufficiently been incorporated in BEF theories and experimentally tested [54,56]. We suggest that an integrative, hierarchical approach combining protists, BALOs and phages should be developed to exploit their potential to remove pathogens and reduce microbial loads from wastewater. In addition to improving an essential environmental technology, this could lead to an integrated mechanistic understanding of predatory interactions at the micro-scale with far reaching implications on the functioning of ecosystems.
Acknowledgement This work was funded by the German Research Foundation grant CH 731/2-1. Current Opinion in Biotechnology 2014, 27:185–190
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ScienceDirect Multiple micro-predators controlling bacterial communities in the environment Julia Johnke1, Yossi Cohen2, Marina de Leeuw3, Ariel Kushmaro3, Edouard Jurkevitch2 and Antonis Chatzinotas1 Predator–prey interactions are a main issue in ecological theory, including multispecies predator–prey relationships and intraguild predation. This knowledge is mainly based on the study of plants and animals, while its relevance for microorganisms is not well understood. The three key groups of micro-predators include protists, predatory bacteria and bacteriophages. They greatly differ in size, in prey specificity, in hunting strategies and in the resulting population dynamics. Yet, their potential to jointly control bacterial populations and reducing biomass in complex environments such as wastewater treatment plants is vast. Here, we present relevant ecological concepts and recent findings on micropredators, and propose that an integrative approach to predation at the microscale should be developed enabling the exploitation of this potential. Addresses 1 Department of Environmental Microbiology, Helmholtz Centre for Environmental Research - UFZ, 04318 Leipzig, Germany 2 Department of Plant Pathology and Microbiology, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, 76100 Rehovot, Israel 3 Department of Biotechnology Engineering and The National Institute for Biotechnology, Ben Gurion University, 84105 Beer Sheva, Israel Corresponding author: Jurkevitch, Edouard ([email protected])
Current Opinion in Biotechnology 2014, 27:185–190 This review comes from a themed issue on Environmental biotechnology Edited by Hauke Harms and Howard Junca
0958-1669/$ – see front matter, # 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.copbio.2014.02.003
Introduction Predation is a major mode of interaction between organisms in the living world, with predators spanning from the submicron level (bacteriophages) to meters in size [1]. Predation in macro-organisms has been the subject of many studies but our understanding of its importance at the microscale is lacking. Microbes constitute the largest biomass of organisms on Earth. Accordingly, the microbial food web has been shown to be a main driver of the planet’s biogeochemical cycles, controlling nutrient recycling and trophic transfer of the major six elements H, C, www.sciencedirect.com
N, O, S and P [2]. Although predatory interactions between microbes appear to be the largest factor of bacterial mortality in many ecosystems [3,4], there is still a considerable gap of knowledge on the processes they affect, and of their dynamics at the microscale. Filling this gap requires bringing together classical ecological theory and the understandings of the particulars of organisms at this scale. Consequently, questions resulting from predator–prey interactions such as the role of multispecies predator– prey systems [5] or more recently the question, how diversity affects ecological processes [6], that is, the relation between biodiversity and ecosystem function (BEF) should be addressed in this context. A recent meta-analysis has revealed a general positive mean predator (secondary consumers) richness effect on prey suppression, though species identity seems to contribute substantially to the variability observed in experiments [7]. Niche complementarity, overexploitation of prey, reduction in prey species richness and consequently reduced prey production, or dominance by less competitive prey species are potential mechanisms by which increasing predator diversity can decrease total prey biomass [8]. Differences in prey use patterns can produce saturating (i.e. maximum redundancy), additive (i.e. maximum complementarity) or mixed effects [9], whereas antagonistic interactions may negatively affect consumption rates of prey [10]. Particularly, the prey range of a predator (i.e. generalist or specialist) may largely determine the importance of top-down control as compared to a resource driven bottom-up control of the prey [11]. An important aspect in the context of multiple predation is to know whether or not intraguild predation (IGP) occurs in a given habitat. IGP combines aspects of predation and competition and refers to predation among two predator species which also compete for the same prey [12,13]. Such negative interactions strongly impact predator-diversity effects and eventually result in lowered prey suppression rates; moreover IGP effects vary across different ecosystems [12], while densities of alternative prey resources may affect the strength of IGP [14]. Likewise, it is equally important to address the role of prey species diversity on the strength of top-down control. Several potential mechanisms have been proposed so far: predation-resistant or inedible species can dominate Current Opinion in Biotechnology 2014, 27:185–190
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mixed assemblages, while diverse resources can reduce the efficiency of specialist consumers or provide a more complete range of nutritional resources, resulting in higher consumer biomass and top-down control [8,15,16]. Similarly, the production of toxic substances by a cooperating bacterial community can protect neighboring, non-toxic bacteria from predation. This may facilitate the establishment of predation-sensitive bacteria and may lead to an increased bacterial diversity [17].
Predatory key players at the microscale At the microscale, three key players convey these interactions: eukaryotic protists, predatory bacteria and bacteriophages. Protists are ubiquitous and overall generalist grazers of prokaryotes in marine, aquatic and terrestrial ecosystems. They represent one of the major factors accounting for the mortality of prokaryotes in the environment [2] greatly affecting microbial nutrient recycling and regeneration. A key aspect of this predatory interaction is the removal of a high number of bacteria in a short amount of time. In laboratory settings soil protists require between 129 and 12,000 bacteria per cell division [18]. The protistan community in natural ecosystems follows a successional pattern depending on the nature of the grazer. For example, early biofilm colonizers (or generalists, including flagellates and ciliates) are highly mobile, allowing fast surface feeding, while intermediate late colonizers (some ciliates and amoebas) are classified as specialists and are abundant in mature biofilms [19]. Protists further differ in feeding strategies by showing prey preferences (depending on bacterial size, motility, shape, cell surface characteristics and food quality [20,21]), which is one explanation, why different bacterivorous protists coexist in the same habitat. Molecular environmental surveys have revealed that protistan communities are much more diverse than previously assumed [22]. Even closely related and morphologically similar strains show high functional diversity and have different impact on prey communities [23]. Although experimental manipulation of protistan grazing pressure was found to induce shifts in bacterial community structure [21], direct analyses of predatory protist–prey interactions are still rare. With the development of new tools enabling, for example, the tracking of stable isotopelabeled prey cells [24,25] we can hopefully gain new insights in the future. Consistent with the keystone predation model, predation resistant and vulnerable species coexist at intermediate productivities [26]; negative selection effects at higher productivity lead to a stronger selection of predation resistant, albeit unproductive species [27], and thus a decline in prey diversity. The diet breadth of a predator (generalist vs. specialist) can also change the relative strength of bottom-up and top-down forces in bacterial communities, though current data probably do not allow a Current Opinion in Biotechnology 2014, 27:185–190
generalization [28]. Moreover, increasing protist species richness may result in an increase in prey evenness, probably due to the reduction of competitive interactions and the growth of subdominant species in diverse bacterial systems [29]. In accordance with current ecological theories, prey resources are more substantially reduced when exposed to a diverse set of protists with different feeding modes [29], pointing to complementarity effects in multi-predator assemblages [30]. Recent evidence that presence of an intraguild prey may even induce trophic polymorphisms of freshwater ciliates, points to a phenotypic plasticity that allows organisms to adapt to changes in the environment, with consequences for the diet breath and the community dynamics [31]. Bacteriophages (phages) in aquatic ecosystems can reach densities 10–100 times higher than bacteria [4], with viral lysis being responsible for up to 71% of bacterial mortality [32]. As opposed to protists, phages are mostly highly host-specific, a characteristic that may lead to oscillations in both predator and prey as suggested by the ‘killing the winner’ hypothesis: bacterial populations are affected in a density dependent manner so that the most abundant bacteria are preferentially targeted [33], thereby maintaining microbial diversity [34]. Another hypothesis, antagonistic coevolution claims that bacterial strains develop resistance to bacteriophages attacking them [35], leading to an arms-race [36,37]. Indeed, Pal et al. [38] showed that bacteria with high mutation rates are selected in the presence of bacteriophages. Rapid mutations in both populations may also lead to oscillatory dynamics in microbial populations. Yet, more complex bacteriophage-driven effects may be at play as bacterial killing may also contribute nutrients through the release of prey breakdown products, bringing about bacterial growth [39]. Bacteriophages can also act as defense agents for bacteria under protist predation pressure [40]. For instance, the phage-encoded Shiga toxin (Stx) negatively impacted a Tetrahymena thermophila population in a lab experiment. Bacteria containing the toxin-encoding phage showed a survival advantage over bacteria that were not infected. A similar mechanism was observed for Acanthamoeba in coculture with phage-infected Corynebacterium diphteriae. Here, intoxication only occurred when the exotoxin was released after the internalization of the bacteria by the amoeba. Therefore, bacteria can use phages to function as ‘Trojan horse’ in order to survive protist attacks (dotted lines in Figure 2). Predatory bacteria include obligate as well as facultative predators. The former are constituted of several genera collectively known as the Bdellovibrio and like organisms (BALOs), which prey on many Gram negative bacteria, and are ubiquitously distributed in terrestrial and aquatic environments [41]. BALOs are periplasmic (i.e. they www.sciencedirect.com
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penetrate, grow and divide within the prey [42]) or epibiotic (they attach to the cell wall, and grow and divide outside the prey [41]) (Figure 1). By contrast to the generalist nature of protist predation, and the specific interactions of phages with their hosts, BALOs are neither true generalist nor hard-core specialists [43]. Instead, prey range differs between isolates, being more or less broad. Consequently, the overall breath of BALO prey is unknown and the impact of BALOs on bacterial communities not defined. Experimental manipulations of BALO prey interactions have shown that the addition of a specific prey into natural samples leads to specific responses in BALO populations [43], more complex than the ‘killing the winner’ patterns observed in wastewater phages [34]. Furthermore, Shemesh et al. [44] showed that BALOs do not eradicate prey from cultures as prey populations exhibit phenotypic plasticity leading to increased resistance to predation, and Gallet et al. [45,46] demonstrated that BALOs and prey rapidly evolve to yield populations varying in predatory and resistance capabilities, respectively. Although ubiquitous, BALOs are only one component of the ill-defined bacterial predatory community. Recent genome-based studies have shown that specific molecular signatures are found in predatory bacteria, opening the way for a better classification of predatory activity in ecosystems and the uncovering of novel predators [47].
Perspectives of integrated micro-predation research In WWTPs heterotrophic communities efficiently remove organics, nutrients, toxic substances, and pathogens. The very nature of micro-predation can potentially improve wastewater treatment by specifically removing bacterial pathogens (by BALOs and phages) or by reducing the
overall bacterial load (by BALOs and protists). As an example, protists can filter as much as 1000 nl/h, implying that the entire liquid of an activated sludge plant can be filtered in less than 1 h [48]. Yet, crucially assessing phenomena such as prey preferences, environmental effects, and IGP, in relation to a system’s productivity, constitute crucial goals for a reliable application in biotechnological settings such as WWTP [49]. Most interactions between the here presented micro-predator groups remain understudied [60,62,64]; even more importantly, their combined effects on bacterial communities are unknown (Figure 2). Network analyses have recently been shown to allow untangling interactions and co-occurrence patterns within complex microbial communities and revealing environmental conditions that correlate with these relationships [50]. So far, by contrast to protist [48], few studies on waste water treatment processes have included phages or BALOs [51]. Bacteriophages have been widely searched for and detected in WWTP [34,52] because of their capacity to affect the bacterial community [34]. This was shown in the dewatering of sludge which is improved by using phages to degrade the bacterially produced exopolysaccharide, aiding floc formation [53,61]. Furthermore, phages can be used to reduce excess biological sludge and excess foaming [55]. Using Fluorescence in Situ Hybridization (FISH) on waste water sludge flocks samples, Dolinsek et al. [51] demonstrated interactions of the BALO Micavibrio with the nitrite-oxidizing bacteria, sub-lineage I Nitrospira cluster. Although only about 4% of the sub-lineage I Nitrospira aggregates were surrounded by Micavibrio-like bacteria, it was posited that the predators may prevent any particular nitrifier strain from becoming dominant, thus driving diversification,
Figure 1
500nm
1 µm
1 µm
Current Opinion in Biotechnology
Bdellovibrio bacteriovorus (a periplasmic predator) within an Escherichia coli prey (left); Bdellovibrio exovorus (an epibiotic predator) attached to a Caulobacter crescentus prey (right). www.sciencedirect.com
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References and recommended reading
Figure 2
Papers of particular interest, published within the period of review, have been highlighted as:
IGP
of special interest of outstanding interest
Protists
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Possible interactions among protists, BALOs and phages in multipredator communities. Although some of the pictured interactions have been described already, others are severely understudied (dashed lines). Protists have been shown in a few cases to affect virus (phage) populations either indirectly by feeding on infected bacteria (coincidental IGP [57]) or by direct grazing on virus-like particles (omnivorous IGP [58]). Vice versa, viruses are likely to infect heterotrophic protists with yet unclear consequences for top-down control of bacteria [59] or use bacteria as ‘Trojan horse’ in order to kill protists (dotted line) [40]. BALOs, like other bacteria, can be infected with phages [63,65], while any direct interaction with protists is unknown. All of the three micropredators graze on bacteria, though, with different prey range from highly specific (phages) up to rather unspecific predation (protists) as indicated by the thickness of the arrows.
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Conclusions We believe that development of biologically realistic models of trophic interactions in diverse systems and subsequently appropriate management strategies (as in WWTPs) will require the unification of research on BEF, functional traits, predator and prey habitats, and how these interact with environmental heterogeneity and complexity [54]. Several predator and prey traits including microhabitat use, mobility and patchy distribution, feeding niches and behavior have only insufficiently been incorporated in BEF theories and experimentally tested [54,56]. We suggest that an integrative, hierarchical approach combining protists, BALOs and phages should be developed to exploit their potential to remove pathogens and reduce microbial loads from wastewater. In addition to improving an essential environmental technology, this could lead to an integrated mechanistic understanding of predatory interactions at the micro-scale with far reaching implications on the functioning of ecosystems.
Acknowledgement This work was funded by the German Research Foundation grant CH 731/2-1. Current Opinion in Biotechnology 2014, 27:185–190
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