The role of productivity in the ecological and evolutionary dynamics of predator-prey interaction

Productivity is predicted to drive the ecological and evolutionary dynamics of predator-prey interaction through changes in resource allocation between different traits. However, resources are seldom constantly available and thus temporal variation in productivity could have considerable effect on the species' potential to evolve. To study this, three long-term microbial laboratory experiments were established where Serratia marcescens prey bacteria was exposed to predation of protist Tetrahymena thermophila in different prey resource environments. The consequences of prey resource availability for the ecological properties of the predator-prey system, such as trophic dynamics, stability, and virulence, were determined. The evolutionary changes in species traits and prey genetic diversity were measured. The prey defence evolved stronger in high productivity environment. Increased allocation to defence incurred cost in terms of reduced prey resource use ability, which probably constrained prey evolution by increasing the effect of resource competition. However, the magnitude of this trade-off diminished when measured in high resource concentrations. Predation selected for white, non-pigmented, highly defensive prey clones that produced predation resistant biofilm. The biofilm defence was also potentially accompanied with cytotoxicity for predators and could have been traded off with high motility. Evidence for the evolution of predators was also found in one experiment suggesting that co-evolutionary dynamics could affect the evolution and ecology of predator-prey interaction. Temporal variation in resource availability increased variation in predator densities leading to temporally fluctuating selection for prey defences and resource use ability. Temporal variation in resource availability was also able to constrain prey evolution when the allocation to defence incurred high cost. However, when the magnitude of prey trade-off was small and the resource turnover was periodically high, temporal variation facilitated the formation of predator resistant biofilm. The evolution of prey defence constrained the transfer of energy from basal to higher trophic levels, decreasing the strength of top-down regulation on prey community. Predation and temporal variation in productivity decreased the stability of populations and prey traits in general. However, predation-induced destabilization was less pronounced in the high productivity environment where the evolution of prey defence was stronger. In addition, evolution of prey defence weakened the environmental variation induced destabilization of predator population dynamics. Moreover, protozoan predation decreased the S. marcescens virulence in the insect host moth (Parasemia plantaginis) suggesting that species interactions outside the context of host-pathogen relationship could be important indirect drivers for the evolution of pathogenesis. This thesis demonstrates that rapid evolution can affect various ecological properties of predator-prey interaction. The effect of evolution on the ecological dynamics depended on the productivity of the environment, being most evident in the constant environments with high productivity.Ympäristön tuottavuuden ennustetaan vaikuttavan peto-saalissuhteen ekologiseen ja evolutiiviseen dynamiikkaan eri ominaisuuksiin allokoitavien resurssien määrän kautta. Resurssien saatavuus vaihtelee kuitenkin usein ajallisesti, jolla voi olla suuri merkitys lajien evoluutiopotentiaalille. Tutkin väitöskirjassani resurssiympäristön merkitystä peto-saalissuhteen evoluutioon kolmessa pitkäaikaisessa mikrokosmoskokeessa, jossa altistin saalisbakteeri Serratia marcescens:ia alkueläin Tetrahymen thermopila:n saalistukselle. Kokeissa mitattiin lajien evolutiivisia muutoksia ja niiden vaikutusta peto-saalisyhteisön ekologisiin ominaisuuksiin (kuten trofia-dynamiikkaan, stabiliteettiin, diversiteettiin ja saaliin virulenssiin). Saalisbakteerin puolustuskyky kehittyi erityisen vahvaksi ympäristöissä, joiden tuottavuustaso oli korkea. Saaliin puolustuskyvyn parantuminen vähensi kuitenkin saaliin resurssienkäyttötehokkuutta, mikä rajoitti saaliin puolustuskyvyn evoluutiota kun ympäristön tuottavuustaso oli alhainen. Mittausravintokonsentraation kasvattaminen vähensi puolustuksen ja resurssinkäyttötehokkuuden välisen allokaatiokustannuksen merkitystä saaliin kelpoisuudelle. Resurssien saatavuuden ajallinen vaihtelu lisäsi petojen populaatiokokojen varianssia, mikä johti saalisbakteereihin kohdistuvien valintapaineiden vaihtelun lisääntymiseen. Resurssien saatavuuden ajallinen vaihtelu rajoittikin saaliin puolustuskyvyn evoluutiota, kun tästä aiheutunut kustannus saaliin kilpailukyvyssä oli iso. Resurssien saatavuuden ajallisella vaihtelulla oli sen sijaan pienempi merkitys, kun resurssien virtaus oli suuri ja saaliin puolustuksen parantamisesta aiheutuva kustannus kilpailukyvyssä oli pieni. Pedot valikoivat etenkin valkoisia pesäkkeitä muodostavia, tehokkaasti puolustautuvia saalisbakteerityyppejä, jotka kasvoivat alkueläimille huonosti ravinnoksi kelpaavana biofilminä (bakteerien kasvu solurykelminä kasvatusastioiden pinnoilla). Lisäksi biofilmeissä muodostui mahdollisesti alkueläimille myrkyllisiä yhdisteitä ja staattinen kasvumuoto saattoi olla syynä bakteerien vähentyneelle liikkumiselle. Myös pedot pystyivät kehittymään paremmiksi saalistajiksi, mutta vain yhdessä kokeistani, jossa resurssien virtaus oli suurin. Saaliin evolutiiviset muutokset vaikuttivat moniin peto-saalissuhteen ekologisiin ominaisuuksiin. Saaliin puolustuskyvyn evoluutio esimerkiksi rajoitti energian siirtymistä ravintoketjun ylimmälle trofiatasolle, mikä heikensi petojen merkitystä saalispopulaatiokokojen säätelyssä. Saalistus ja resurssien saatavuuden ajallinen vaihtelu lisäsivät yleisesti saaliin ominaisuuksien ja lajien populaatiokokojen vaihtelua. Saalistuksen epästabiloiva vaikutus ei kuitenkaan ollut niin vahvaa, kun ympäristön tuottavuustaso oli korkea. Lisäksi saaliin puolustuskyvyn evoluutio vähensi ympäristön vaihtelun kasvattamaa populaatiodynamiikan vaihtelua. Alkueläinten saalistuksen aiheuttamat evolutiiviset muutokset laskivat myös saalisbakteerin virulenssia Parasemia plantaginis täpläsiilikäs-isännässä. Isäntä-patogeenisuhteen ulkopuoliset lajivuorovaikutukset voivatkin olla tärkeitä, epäsuoria, bakteerin virulenssin evoluutioon vaikuttavia tekijöitä. Tämä väitöskirja havainnollistaa, että lajien evoluutio voi olla kyllin nopeaa vaikuttaakseen lukuisiin peto-saalissuhteen ekologisiin ominaisuuksiin. Evoluution merkitys peto-saalissuhteen ekologiselle dynamiikalle näyttäisi kuitenkin riippuvan erityisesti ympäristön tuottavuudesta sen ollessa selkeintä silloin, kun resursseja on jatkuvasti saatavilla ja ympäristön tuottavuustaso on korkea

Protist predation can favour cooperation within bacterial species

Here, we studied how protist predation affects cooperation in the opportunistic pathogen bacterium Pseudomonas aeruginosa, which uses quorum sensing (QS) cell-to-cell signalling to regulate the production of public goods. By competing wild-type bacteria with QS mutants (cheats), we show that a functioning QS system confers an elevated resistance to predation. Surprisingly, cheats were unable to exploit this resistance in the presence of cooperators, which suggests that resistance does not appear to result from activation of QS-regulated public goods. Instead, elevated resistance of wild-type bacteria was related to the ability to form more predation-resistant biofilms. This could be explained by the expression of QS-regulated resistance traits in densely populated biofilms and floating cell aggregations, or alternatively, by a pleiotropic cost of cheating where less resistant cheats are selectively removed from biofilms. These results show that trophic interactions among species can maintain cooperation within species, and have further implications for P. aeruginosa virulence in environmental reservoirs by potentially enriching the cooperative and highly infective strains with functional QS system

The effects of antibiotic combination treatments on Pseudomonas aeruginosa tolerance evolution and coexistence with Stenotrophomonas maltophilia

Pseudomonas aeruginosa bacterium is a common pathogen of Cystic Fibrosis (CF) patients due to its ability to evolve resistance to antibiotics during treatments. While P. aeruginosa resistance evolution is well characterised in monocultures, it is less well understood in polymicrobial CF infections. Here, we investigated how exposure to ciprofloxacin, colistin, or tobramycin antibiotics, administered at sub-MIC doses alone and in combination, shaped the tolerance evolution of P. aeruginosa (PAO1 lab and clinical CF LESB58 strains) in the absence and presence of a commonly co-occurring species, Stenotrophomonas maltophilia. Increases in antibiotic tolerances were primarily driven by the presence of that antibiotic in the treatment. We observed a reciprocal cross-tolerance between ciprofloxacin and tobramycin, and when combined these antibiotics selected increased MICs for all antibiotics. Though the presence of S. maltophilia did not affect the tolerance or the MIC evolution, it drove P. aeruginosa into extinction more frequently in the presence of tobramycin due to its relatively greater innate tobramycin tolerance. In contrast, P. aeruginosa dominated and drove S. maltophilia extinct in most other treatments. Together, our findings suggest that besides driving high-level antibiotic tolerance evolution, sub-MIC antibiotic exposure can alter competitive bacterial interactions, leading to target pathogen extinctions in multi-species communities.Funding provided by: University of YorkCrossref Funder Registry ID: http://dx.doi.org/10.13039/100009001Award Number:See Methods in paper for collection. MIC values (MIC data.csv) derived from visual inspection of antibiotic growth measurements plotted as a growth curve. Optical density data has been blank-corrected, and in the case of the antibiotic growth measurements (Antibiotic growth data.csv) averaged over ≤3 technical replicates

Life history trade-offs and relaxed selection can decrease bacterial virulence in environmental reservoirs

Pathogen virulence is usually thought to evolve in reciprocal selection with the host. While this might be true for obligate pathogens, the life histories of opportunistic pathogens typically alternate between within-host and outside-host environments during the infection-transmission cycle. As a result, opportunistic pathogens are likely to experience conflicting selection pressures across different environments, and this could affect their virulence through life-history trait correlations. We studied these correlations experimentally by exposing an opportunistic bacterial pathogen Serratia marcescens to its natural protist predator Tetrahymena thermophila for 13 weeks, after which we measured changes in bacterial traits related to both anti-predator defence and virulence. We found that anti-predator adaptation (producing predator-resistant biofilm) caused a correlative attenuation in virulence. Even though the direct mechanism was not found, reduction in virulence was most clearly connected to a predator-driven loss of a red bacterial pigment, prodigiosin. Moreover, life-history trait evolution was more divergent among replicate populations in the absence of predation, leading also to lowered virulence in some of the ‘predator absent’ selection lines. Together these findings suggest that the virulence of non-obligatory, opportunistic bacterial pathogens can decrease in environmental reservoirs through life history trade-offs, or random accumulation of mutations that impair virulence traits under relaxed selection.Peer reviewe

Plant pathogenic bacterium can rapidly evolve tolerance to an antimicrobial plant allelochemical

Crop losses to plant pathogens are a growing threat to global food security and more effective control strategies are urgently required. Biofumigation, an agricultural technique where Brassica plant tissues are mulched into soils to release antimicrobial plant allelochemicals called isothiocyanates (ITCs), has been proposed as an environmentally friendly alternative to agrochemicals. Whilst biofumigation has been shown to suppress a range of plant pathogens, its effects on plant pathogenic bacteria remain largely unexplored. Here, we used a laboratory model system to compare the efficacy of different types of ITCs against Ralstonia solanacearum plant bacterial pathogen. Additionally, we evaluated the potential for ITC‐tolerance evolution under high, intermediate, and low transfer frequency ITC exposure treatments. We found that allyl‐ITC was the most efficient compound at suppressing R. solanacearum growth, and its efficacy was not improved when combined with other types of ITCs. Despite consistent pathogen growth suppression, ITC tolerance evolution was observed in the low transfer frequency exposure treatment, leading to cross‐tolerance to ampicillin beta‐lactam antibiotic. Mechanistically, tolerance was linked to insertion sequence movement at four positions in genes that were potentially associated with stress responses (H‐NS histone like protein), cell growth and competitiveness (acyltransferase), iron storage ([2‐Fe‐2S]‐binding protein) and calcium ion sequestration (calcium‐binding protein). Interestingly, pathogen adaptation to the growth media also indirectly selected for increased ITC tolerance through potential adaptations linked with metabolism and antibiotic resistance (dehydrogenase‐like protein) and transmembrane protein movement (Tat pathway signal protein). Together, our results suggest that R. solanacearum can rapidly evolve tolerance to allyl‐ITC plant allelochemical which could constrain the long‐term efficiency of biofumigation biocontrol and potentially shape pathogen evolution with plants

Seeing the forest for the trees : Use of phages to treat bacterial tree diseases

Trees and woody plants can be attacked by many pests and pathogens either individually or as polymicrobial infections. In particular, infections caused by tree-specific bacterial pathogens have become more common during the last decade, causing serious concern for important tree and woody plant species in horticulture, urban environments, and forests. For example, Xylella and Pseudomonas bacteria are causing significant economic and ecological devastation throughout Europe in olive, cherry, and other stone fruits, mainly because of lack of efficient control methods and the emergence of bacterial resistance to traditional antimicrobial compounds such as copper and antibiotics. Hence, there is an urgent need for innovative approaches to tackle bacterial plant diseases. One way to achieve this could be through the application of biological control, which offers a more environmentally friendly and targeted approach for pathogen management. This review will explore recent advances in use of pathogen-specific viruses, bacteriophages (or phages), for the biocontrol of bacterial tree diseases. Phages are an important component of plant microbiomes and are increasingly studied in plant pathogen control due to their highly specific host ranges and ability to selectively kill only the target pathogenic bacteria. However, their use still poses several challenges and limitations, especially in terms of managing the bacterial diseases of long-lived trees. A particular insight will be given into phage research focusing on controlling Pseudomonas syringae pathovars, Erwinia amylovora, Xanthomonas species, Ralstonia solanacearum, and Agrobacterium tumefaciens. Recent milestones, current challenges, and future avenues for phage therapy in the management of tree diseases are discussed

Interactive effects between diet and genotypes of host and pathogen define the severity of infection

Host resistance and parasite virulence are influenced by multiple interacting factors in complex natural communities. Yet, these interactive effects are seldom studied concurrently, resulting in poor understanding of host-pathogen-environment dynamics. Here, we investigated how the level of opportunist pathogen virulence, strength of host immunity and the host condition manipulated via diet affect the survival of wood tiger moth Parasemia plantaginis (Arctidae). Larvae from “low cuticular melanin” and “high cuticular melanin” (considered as low and high pathogen resistance, respectively) selection lines were infected with moderately and highly virulent bacteria strains of Serratia marcescens, while simultaneously manipulating host diet (with or without antibacterial compounds). We measured host survival and food preference before and after infection to test whether the larvae “self-medicate” by choosing an anti-infection diet (Plantago major, i.e., plantain leaf) over lettuce (Lactuca sativa). “High melanin” larvae were more resistant than “low melanin” larvae to the less virulent strain that had slower growth and colonization rate compared with the more virulent strain. Cuticular melanin did not enhance survival when the larvae were infected with the highly virulent strain. Anti-infection diet enhanced survival of the “high melanin” but not the “low melanin” hosts. Survival was dependent on family origin even within the melanin selection lines. Despite the intrinsic preference for lettuce, no evidence of self-medication was found. These results demonstrate that the relative benefit of host cuticular melanin depends on both diet and pathogen virulence: plantain diet only boosted the immunity of already resistant “high melanin” hosts, and cuticular melanin increased host survival only when infected with moderately virulent pathogen. Moreover, there was considerable variation in host survival between families within both melanin lines suggesting genetic basis for resistance. These results indicate that although melanin is an important predictor of insect immunity, its effect on disease outcomes greatly depends on other interacting factors.Peer reviewe

Ecology and evolution of antimicrobial resistance in bacterial communities

Accumulating evidence suggests that the response of bacteria to antibiotics is significantly affected by the presence of other interacting microbes. These interactions are not typically accounted for when determining pathogen sensitivity to antibiotics. In this perspective, we argue that resistance and evolutionary responses to antibiotic treatments should not be considered only a trait of an individual bacteria species but also an emergent property of the microbial community in which pathogens are embedded. We outline how interspecies interactions can affect the responses of individual species and communities to antibiotic treatment, and how these responses could affect the strength of selection, potentially changing the trajectory of resistance evolution. Finally, we identify key areas of future research which will allow for a more complete understanding of antibiotic resistance in bacterial communities. We emphasise that acknowledging the ecological context, i.e. the interactions that occur between pathogens and within communities, could help the development of more efficient and effective antibiotic treatments