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Bacteriophage ecology in environmental biotechnology processes Orr H Shapiro and Ariel Kushmaro Heterotrophic bacteria are an integral part of any environmental biotechnology process (EBP). Therefore, factors controlling bacterial abundance, activity, and community composition are central to the understanding of such processes. Among these factors, top-down control by bacteriophage predation has so far received very limited attention. With over 108 particles per ml, phage appear to be the most numerous biological entities in EBP. Phage populations in EBP appear to be highly dynamic and to correlate with the population dynamics of their hosts and genomic evidence suggests bacteria evolve to avoid phage predation. Clearly, there is much to learn regarding bacteriophage in EBP before we can truly understand the microbial ecology of these globally important systems. Address Ben Gurion University of the Negev, Biotechnology Engineering, POb 653, Beer sheva 84105, Israel Corresponding author: Shapiro, Orr H (
[email protected])
Current Opinion in Biotechnology 2011, 22:1–7 This review comes from a themed issue on Environmental biotechnology Edited by Lindsay Eltis and Ariel Kushmaro
0958-1669/$ – see front matter # 2011 Elsevier Ltd. All rights reserved. DOI 10.1016/j.copbio.2011.01.012
Introduction Heterotrophic bacteria are an integral part of any environmental biotechnology process (EBP). This is particularly true for wastewater treatment processes (WWTP), where bacteria play key roles in nutrient removal and the transformation and mineralization of organic matter. Therefore, factors controlling bacterial abundance, activity, and community composition are central to the understanding of such processes. Among these factors, top-down control through viral lysis has so far received very limited attention. Bacteriophage (viruses attacking bacteria) are considered to be the most abundant and diverse biological entities on earth, with ten phages for every bacterial cell in most studied ecosystems [1]. The strong predation pressure exerted by phage on microbial communities means that bacterial fitness is measured by their adaptation not only to available resources but also to the biotic environment www.sciencedirect.com
[2]. Bacteriophage are therefore continuously regulating microbial ecology and activity, including carbon and nutrient fluxes, food web dynamics, and microbial diversity and diversification [3,4]. While the number of studies directed towards bacteriophage ecology in aquatic systems is rapidly rising over the past decade, surprisingly few studies target phage ecology in WWTP. The current review aims to bring the reader up-to-date with what little is known, introduce some theories regarding possible effects of phage activity on WWTP microbial ecology and suggest possible directions for future study.
Viruses in wastewater treatment processes Viruses, including bacteriophage, are long known to be found in EBP such as activated sludge WWTP [5] but most studies in this field either disregard them completely or focus on the detection of viral particles in treated wastewater as indicators of survival and release of pathogenic viruses into the environment [6–8]. Bacteriophage ecology in WWTP was first considered in two separate studies published three decades ago [9,10], yet a search of the scientific literature today still returns less than 20 publications specifically targeting this subject. Consequently, our knowledge and understanding of phage ecology in WWTP, and their potential influence on these globally important processes, are still inadequate.
How many are there? When studying phage in the environment, this is often one of the first questions asked. While the answer in itself does little to promote our understanding of phage ecology, it gives a measure of their significance in the microbial process (the more there are the more important they must be) and enables back-of-the-envelope calculations resulting in impressively big numbers. Indeed, it was the number of phage in the environment that first drew the attention of the scientific community to their central place in microbial ecology [4,11,12]. Otawa et al. applied epifluorescence microscopy (EFM) to estimate total viral counts in 18 full scale activated sludge bioreactors, reporting viral concentrations of 108 to 109 virus like particles (VLP)/ml. Similar values were obtained for a municipal wastewater treatment plant in Singapore [13] and for a continuous flow, two stage bioreactor in Israel [14]. These studies suggest viral abundance in activated sludge to be higher than any other environment studied to date [15]. The ratio of VLP to bacterial cells in WWTP was shown to approximate 10:1 [14], that is, similar to values obtained from Current Opinion in Biotechnology 2011, 22:1–7
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other environments, [4,16] indicating similar levels of activity. When considering the impact of bacteriophage on other aquatic environments [16] surely this activity deserves more attention than that given to it so far.
What can we say of their diversity? As phage are obligate parasites, their diversity in a given environment is necessarily limited by the presence of their prey. Based on the assumption that each bacterial species is infected by at least one phage, it is reasonable to assume bacteriophage diversity to be at least as high as bacterial diversity and probably higher [4]. However, bacteriophage diversity is an elusive concept due to a lack of a practical means of measuring it, as well as to the difficulty in defining a viral species [3]. Phage diversity in EBP environments was estimated in several studies using pulsed field gel electrophoresis (PFGE) [13,15] for separating phage populations based on genome size. Using this approach, phage communities composition were shown to vary between different treatment plants and over time in a laboratory bioreactor [15] as well as between the different stages of a full scale treatment process [13]. This method enables the comparison of phage community composition and possibly richness. However, as only highly abundant genomes are detected using this approach, and as phage with similar genome size are not separated, it is unlikely to provide a good estimation of viral diversity. A more promising approach for the elucidation of viral diversity is viral metagenomics, providing a relatively unbiased view of viral communities with the coverage limited primarily by the number of sequences and the quality of subsequent bioinformatic analysis [17]. This approach provides new insights into viral diversity and ecology [18,19] and is likely to become even more central in coming years with the accumulation of annotated viral genomes in genomic databases and the development of dedicated bioinformatic tools for the analysis of the large amount of data generated by metagenomic surveys. In a comparison between the viral metagenome of an activated sludge bioreactor and 16S rRNA gene clone library from the same environment [20], all bacterial phyla from the clone library were represented by sequences in the viral metagenome. Four phyla found in the viral metagenome that were not represented in the clone library were likely the result of insufficient sampling of the bacterial community. As the viral metagenome in that study was limited in size it did not allow for a detailed examination of the viral community. Furthermore, the study only analysed a single time point, wheras viral communities in EBP appear to be highly dynamic [21,22]. Future studies of this type are likely to employ advanced sequencing techniques and Current Opinion in Biotechnology 2011, 22:1–7
should target multiple time points in order to gain a meaningful insight into the viral diversity and ecology of EBP.
Are they all active? In contrast to the large number of phage-like particles detectable using EFM, viable counts as plaque-forming units (PFU), that is, the number of plaques formed on a given bacterial host per unit volume, is typically considerably lower, in the range of 103 to 104 PFU/ml [4]. PFU counts from wastewater treatment bioreactors, for bacterial hosts isolated from the same location, are typically between 102 and 104 PFU/ml [22–24], with the highest reported count at approximately 4 105 PFU/ ml [21]. However, several studies have shown PFU counts to vary with time [10,21,22,24], so that no single measurement can reflect the true abundance of phage attacking a given bacterial strain. The reason for the observed discrepancy between direct and viable counts, also termed the ‘Great-Plaque-CountAnomaly’ [4], is unclear. It may be that the majority of phage observed by direct counts are not viable, or that many are unable to form plaques in a PFU assay. An alternative explanation is that each bacterial strain is only susceptible to a small part of the bacteriophage community, with each bacterial ‘species’ subdivided into multiple serotypes separated by their susceptibility to different phage. The observed ratio between direct and viable counts therefore implies an immense level of microdiversity within both viral and bacterial communities, and accordingly highly complex interactions between the various microbial groups.
What are they doing? I: killing the winner While bacteriophage are indisputably abundant in all microbial environments, their precise place in microbial ecology is still inadequately understood. A commonly accepted model to describe phage–host interactions is that of ‘killing the winner’ (KtW) [25,26]. This model that is based on Lotka-Volterra-type equations predicts negative frequency-dependent selection of microbial populations to be the main force driving phage–host interactions [27]. This simplified model has been demonstrated under laboratory settings (e.g. [28]) but is generally hard to demonstrate for complex microbial communities due to the need for identification of a phage–host system that is sufficiently dominant in the studied environment. One possible prediction from this model is the periodical rise and fall of specific microbial populations due to specific phage–host interactions (Figure 1c). A pattern consistent with this model was recently demonstrated in a full scale membrane bioreactor treating industrial wastewater, where PFU counts on several bacterial strains appeared to oscillate in correlation with their potential hosts [21]. A similar pattern was reported for a host strain inoculated into a laboratory scale bioreactor and its phage [24]. Abundance of phage www.sciencedirect.com
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Figure 1
WWTP are fluctuating together with their specific phage as predicted by KtW.
(a)
(b)
An intrinsic assumption in KtW models is that each phage parasites a specific bacterial lineage [27]. Contrastingly, several studies demonstrate phage isolated from EBP to be polyvalent, that is, able to infect several bacterial hosts. Polyvalent viruses are mostly found to infect several strains of a single species [29]. However, phage isolates were found to infect hosts from different bacterial classes (Shapiro, unpublished data) as well as bacterial isolates with different gram staining [23,30]. Polyvalency was found for all 8 phage isolated from a bench scale activated sludge bioreactor [30] and for 60–90% of phage isolated from EBP in several other studies [21,23,31]. In a study of phage specific to Pseudomonas aeruginosa, phage isolates were obtained from river and lake water and from WWTP [32]. When tested against 40 P. aeruginosa strains, all phage isolates were shown to be polyvalent, with phage originating from WWTP displaying wider host ranges compared to phage from other environments. These observations suggest phage polyvalency should be incorporated into future KtW and other food-web models, both for EBP and for other environments.
(c) τ2
Phage/Host abundance
τ1
Time
Temperature shift or toxic substance
(d)
X
Y
What are they doing? II: antagonistic coevolution
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Current Opinion in Biotechnology
Bacteriophage in wastewater treatment: (a) Transmission electron microscope (TEM) imaging of a thin section (150 nm) through an activated sludge floc. Phage particles are released from a lysed bacterial cell (bar = 500 nm). (b) TEM imaging of a negatively stained phage particle isolated from same activated sludge biomass as in A (bar = 50 nm). (c) Schematic diagram of the population dynamics of phage–hosts systems in a full scale activated sludge reactor. t1 indicates time between peak abundance of the host (green) and phage (red), estimated at 40–60 days (based on [21]). t2 indicates time of infection cycle (time between first and last detection of phage in activated sludge samples). Typical estimates are between 20 and 120 days (based on [10,21,22]). (d) Suggested mechanism for influence of lysogenic infection on process performance. Lysogenic phage infecting one or more bacterial populations carrying out specific metabolic function(s) are induced by sudden temperature shift or the introduction of a toxic substance. Sudden lysis of the bacterial populations causes loss of metabolic function(s) and subsequently may affect process performance.
populations was shown to fluctuate in several other fullscale WWTP [15,22], presumably in response to changes in the abundance of their potential hosts. These findings seem to indicate that dominant bacterial groups in www.sciencedirect.com
An alternative mechanism for phage host interactions is antagonistic coevolution (ACE) [33], that is, an ongoing arms race where hosts are continuously evolving immunity to phage infection while phage evolve to counteract this immunity. Possible evidence for such a process was found for two bacterial communities from phosphate-removing laboratory-scale bioreactors operated in the US and Australia [34]. Both communities showed high viral activity and were found to be highly similar based on phylogenetic analysis. Metagenomic analysis revealed some variation between the communities, mostly at genes related to extracellular polymeric substances (EPS) expression and to clustered regularly interspaced short palindromic repeats (CRISPR) elements, both serving as defense mechanisms against phage predation [35,36]. The authors concluded that the two communities were each adapted to local phage predation, thus demonstrating the importance of phage predation and phage–host coevolution in shaping the microbial communities of WWTP. Intriguingly, duration of the apparent infection cycles (time between first and last detection of a specific phage; see Figure 1c) in full-scale bioreactors was of the order of weeks rather than hours or days observed in laboratory cultures [10,21,22]. This may be simply due to nutrient limitation inducing longer infection period (time between phage infection and cell lysis) and lower burst sizes (number of phage particles released from an infected cell) [37]. High solids density in the bioreactor may also slow down phage propagation by providing shelter to Current Opinion in Biotechnology 2011, 22:1–7
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bacterial cells and increasing the loss rates of free phage particles [38]. An alternative explanation would be a combination of KtW and ACE, so that infection cycles reported in the above studies (e.g. [21]) in fact represent multiple coevolution steps. Accordingly, the observed decline in host densities towards the end of each infection cycle may in part be attributed to a reduction in host fitness associated with ACE [39]. Two separate studies in wastewater environment [21,22] demonstrate more than one infection cycle for phage targeting a single host, separated by several weeks or months. This suggests that host populations in WWTP may recover following an infection cycle, possibly after the numbers of phage targeting a specific host have been depleted. Whether the hosts in repeated cycles retain a ‘memory’ of previous infections in the form of increased phage resistance remains to be determined.
Can phage predation affect process performance? There is as yet little evidence of phage activity directly affecting WWTP performance. A possible exception is the recent report of higher than expected organic carbon removal in a two-stage bioreactor treating oil-refinery drainage water, where phage predation was suggested to drive a microbial loop reducing cell-bound carbon in the reactor effluents [14]. However, phage predation is generally accepted to drive microbial diversification [2,3,16,34] and higher diversity is expected to promote community resistance to perturbation [40]. It may therefore be argued that the activity of bacteriophage maintains (and to some extent creates) the microbial diversity and functional redundancy that confers stability of performance and resilience to perturbations in WWTP. This hypothesis, however, has not yet been tested. A somewhat different question is the effect of phage activity on specific metabolic processes. Due to the high microbial diversity found in wastewater treatment processes and to the undetermined function of much of that diversity, it is often difficult to directly demonstrate such effects. Exceptions to that rule are nitrification and phosphate accumulation processes, with which a small number of distinct microbial groups are associated. These processes offer unique opportunities to link population dynamics and process performance. Fu et al. reported an attempt to inoculate a laboratory-scale biological aerated filter with a nitrifying bacterial strain [41]. Further analysis indicated that the inoculated strain was rapidly purged from the system. A phage specific to that strain was subsequently isolated from the bioreactor, suggesting phage infection to account for at least part of the bioaugmentation failure. Lee et al. reported the operation of a laboratory scale activated sludge bioreactor following inoculation with a strain of Microlunatus phosphovorus, a phosphate accumuCurrent Opinion in Biotechnology 2011, 22:1–7
lating bacterium isolated from activated sludge [24]. Using fluorescence in situ hybridization (FISH) and PFU counts on the inoculated strain, the authors demonstrated a negative correlation between the population dynamics of the host strain and its specific phage indicating a possible effect on phosphate removal, although such effect was not demonstrated. Recently, Barr et al. reported the possible involvement of bacteriophage in a decrease in phosphate removal from a laboratory-scale bioreactor enriched with ‘candidatus Accumulibacter phosphatis’, a phosphate accumulating bacterium associated with WWTP [42]. Supernatant from the bioreactor was added to two smaller bioreactors inoculated with active biomass. Both bioreactors exhibited decreased performance accompanied by elevated phage counts compared to two control bioreactors without supernatant addition, thus supporting the hypothesis that phage activity was responsible for reduced phosphate removal. To date, no evidence exists for phage predation directly affecting a specific metabolic process in full scale WWTP. This may be due to inadequate research effort, but may also be the result of high microbial diversity found in full scale processes, so that selective lysis of a population carrying out a specific metabolic function is compensated by the activity of competing populations.
Lysogenic infection in WWTP bacteria Lysogenic (or temperate) state describes phage life strategy where the phage genome remains within the host in a dormant stage (prophage) and replicates with it, until a lytic cycle is induced. Percent lysogeny, that is, the percentage of bacterial cells in the community containing an inducible viral genome, varies between undetectable and over 80% for different environments and induction methods [4]. There is evidence to suggest that lysogenic infection is favored under limited nutrient availability, as is the case in the strong competition for resources in activated sludge processes. As prophages (and their hosts) in activated sludge processes are retained in the system, while free phage particles are constantly washed out with the process effluents, lysogeny may confer an ecological advantage in this environment. However, no estimates of percent lysogeny are currently available for WWTP, and the importance of lysogenic life strategy in this environment remains to be determined. A prophage may be induced to become lytic due to a rise in temperature, exposure to UV light or the introduction of toxic substances such as antibiotics into the environment [4]. Foaming, deflocculation and decreased process performance are known outcomes of sudden temperature shifts [43] or wastewater toxicity [44] in WWTP. Massive prophage induction followed the sudden lysis of a large proportion of a microbial community www.sciencedirect.com
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(Figure 1d) will produce similar effects and so cannot be ruled out as a possible cause for this type of process failures.
Conclusions Our current understanding of bacteriophage ecology in EBP is limited. We know that they are highly abundant and so apparently active. Density of specific phage populations appear to fluctuate continuously, presumably in response to changes in population density of their respective hosts. However, we cannot say whether phage predation drives changes in host densities, as predicted by the KtW model. Phage predation appears to impact EBP microbial communities at the genomic level in accordance with ACE theory, but we are yet to understand how this impacts the microbial community. We can say with some confidence that many if not all of the phage in EBP can infect more than one host, but we do not know what enables this polyvalency or what limits it. Most importantly, we do not yet understand how bacteriophage activity affects EBP performance and stability. Clearly, most of the work in this field is still ahead of us. The subject of horizontal gene transfer (HGT) [45], that is, the introduction of foreign genes into a bacterial genome, is frequently discussed in the context of phage–host interactions but has so far received very little attention in the context of EBP. No evidence for HGT was found in two communities of ‘candidatus Accumulibacter phosphatis’ shown to be affected by phage activity [34]. Contrastingly, diverse antimicrobial resistance genes were detected in a metagenomic survey of both bacterial and viral communities from an activated sludge system, indicating possible transfer of these genes between bacterial hosts sharing a common phage [46]. Alternatively, these findings could indicate possible mutualistic relationships between phage and their hosts as lysogenic phage may confer antibiotic resistance to infected cells [47]. Phage have also been shown to carry genes encoding for bacterial proteins [48] while phage activity has been shown to affect specific traits of their bacterial hosts such as pathogenicity [49]. The extent of such interactions in EBP environments and their affect on the microbial community are yet to be studied. The need to integrate ecological principles into the understanding and management of EBP is recognized by both microbial ecologists and environmental engineers [50]. The ultimate goal of microbial ecology studies in EBP is to improve the performance and controllability of the process. Bacteriophage potential and limitations as control agents for the manipulation of WWTP microbial communities have been discussed previously [51] and several attempts to apply phage therapy in EBP have been reported (e.g. [31,52]). However, the complexity of phage–host interactions requires a much better understanding of phage ecology before we can hope to manipwww.sciencedirect.com
ulate or even control them in EBP. Genomic tools available to us today can provide a wealth of information on phage ecology [2,17] including in EBP [20,34]. By using a combination of these tools, in conjunction with isolation-based approaches, to test clear hypotheses it may be possible to overcome part of this complexity and to shed some more light into the ‘black box’ of bacterial and viral ecology in environmental biotechnology processes.
Acknowledgements Y Lichtenfeld and R Jeger assisted with electron microscopy procedures. O Segev and V Shapiro provided useful comments. This work was supported by research funds from the BMBF-MOST Cooperation in Water Technologies Grants WT-501 and WT-901 and a Levi-Eshkol scholarship to OHS from the Israeli Ministry of Science.
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Current Opinion in Biotechnology 2011, 22:1–7
Please cite this article in press as: Shapiro OH, Kushmaro A. Bacteriophage ecology in environmental biotechnology processes, Curr Opin Biotechnol (2011), doi:10.1016/j.copbio.2011.01.012
