Publications by year
2023
Sierocinski P, Bayer F, Hesse E, Buckling A (2023). Rapid evolution drives increased function of a complex microbial community.
Sierocinski P, Stilwell P, Padfield D, Bayer F, Buckling A (2023). The ecology of scale: impact of volume on coalescence and function in methanogenic communities.
Interface Focus,
13(4).
Abstract:
The ecology of scale: impact of volume on coalescence and function in methanogenic communities.
Engineered ecosystems span multiple volume scales, from a nano-scale to thousands of cubic metres. Even the largest industrial systems are tested in pilot scale facilities. But does scale affect outcomes? Here we look at comparing different size laboratory anaerobic fermentors to see if and how the volume of the community affects the outcome of community coalescence (combining multiple communities) on community composition and function. Our results show that there is an effect of scale on biogas production. Furthermore, we see a link between community evenness and volume, with smaller scale communities having higher evenness. Despite those differences, the overall patterns of community coalescence are very similar at all scales, with coalescence leading to levels of biogas production comparable with that of the best-performing component community. The increase in biogas with increasing volume plateaus, suggesting there is a volume where productivity stays stable over large volumes. Our findings are reassuring for ecologists studying large ecosystems and industries operating pilot scale facilities, as they support the validity of pilot scale studies in this field.
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2022
Castledine M, Sierocinski P, Inglis M, Kay S, Hayward A, Buckling A, Padfield D (2022). Greater Phage Genotypic Diversity Constrains Arms-Race Coevolution. Frontiers in Cellular and Infection Microbiology, 12
Castledine M, Padfield D, Sierocinski P, Pascual JS, Hughes A, Mäkinen L, Friman V-P, Pirnay J-P, Vos DD, Buckling A, et al (2022). Parallel phage resistance - virulence trade - offs during clinical phage therapy and in vitro. Access Microbiology, 4(5).
2021
Castledine M, Padfield D, Sierocinski P, Soria Pascual J, Hughes A, Mäkinen L, Friman V-P, Pirnay J-P, Merabishvili M, De Vos D, et al (2021). Parallel evolution of phage resistance - virulence trade - offs during <i>in vitro</i> and nasal <i>Pseudomonas aeruginosa</i> phage treatment.
Abstract:
Parallel evolution of phage resistance - virulence trade - offs during in vitro and nasal Pseudomonas aeruginosa phage treatment
AbstractWith rising antibiotic resistance, there has been increasing interest in treating pathogenic bacteria with bacteriophages (phage therapy). One limitation of phage therapy is the ease at which bacteria can evolve resistance. Negative effects of resistance may be mitigated when resistance results in reduced bacterial growth and virulence, or when phage coevolve to overcome resistance. Resistance evolution and its consequences are contingent on the bacteria-phage combination and their environmental context, making therapeutic outcomes hard to predict. One solution might be to conduct “in vitro evolutionary simulations” using bacteria-phage combinations from the therapeutic context. Overall, our aim was to investigate parallels between in vitro experiments and in vivo dynamics in a human participant. Evolutionary dynamics were similar, with high levels of resistance evolving quickly with limited evidence of phage evolution. Resistant bacteria – evolved in vitro and in vivo - had lower virulence. In vivo, this was linked to lower growth rates of resistant isolates, whereas in vitro phage resistant isolates evolved greater biofilm production. Population sequencing suggests resistance resulted from selection on de novo mutations rather than sorting of existing variants. These results highlight the speed at which phage resistance can evolve in vivo, and in vitro experiments may give useful insights for clinical evolutionary outcomes.
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Sierocinski P, Pascual JS, Padfield D, Salter M, Buckling A (2021). The impact of invader number on whole community invasions in biomethane-producing communities.
Sierocinski P, Soria Pascual J, Padfield D, Salter M, Buckling A (2021). The impact of propagule pressure on whole community invasions in biomethane-producing communities.
iScience,
24(6).
Abstract:
The impact of propagule pressure on whole community invasions in biomethane-producing communities
Microbes can invade as whole communities, but the ecology of whole community invasions is poorly understood. Here, we investigate how invader propagule pressure (the number of invading organisms) affects the composition and function of invaded laboratory methanogenic communities. An invading community was equally successful at establishing itself in a resident community regardless of propagule pressure, which varied between 0.01 and 10% of the size resident community. Invasion resulted in enhanced biogas production (to the level of the pure invading community) but only when propagule pressure was 1% or greater. This inconsistency between invasion success and changes in function can be explained by a lower richness of invading taxa at lower propagule pressures, and an important functional role of the taxa that were absent. Our results highlight that whole community invasion ecology cannot simply be extrapolated from our understanding of single species invasions. Moreover, we show that methane production can be enhanced by invading poorly performing reactors with a better performing community at levels that may be practical in industrial settings.
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2020
Castledine M, Sierocinski P, Padfield D, Buckling A (2020). Community coalescence: an eco-evolutionary perspective.
Philos Trans R Soc Lond B Biol Sci,
375(1798).
Abstract:
Community coalescence: an eco-evolutionary perspective.
Community coalescence, the mixing of different communities, is widespread throughout microbial ecology. Coalescence can result in approximately equal contributions from the founding communities or dominance of one community over another. These different outcomes have ramifications for community structure and function in natural communities, and the use of microbial communities in biotechnology and medicine. However, we have little understanding of when a particular outcome might be expected. Here, we integrate existing theory and data to speculate on how a crucial characteristic of microbial communities-the type of species interaction that dominates the community-might affect the outcome of microbial community coalescence. Given the often comparable timescales of microbial ecology and microevolution, we explicitly consider ecological and evolutionary dynamics, and their interplay, in determining coalescence outcomes. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.
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2019
Dickinson AW, Power A, Hansen MG, Brandt KK, Piliposian G, Appleby P, O'Neill PA, Jones RT, Sierocinski P, Koskella B, et al (2019). Heavy metal pollution and co-selection for antibiotic resistance: a microbial palaeontology approach.
Environment International,
132Abstract:
Heavy metal pollution and co-selection for antibiotic resistance: a microbial palaeontology approach
Frequent and persistent heavy metal pollution has profound effects on the composition and activity of microbial communities. Heavy metals select for metal resistance but can also co-select for resistance to antibiotics, which is a global health concern. We here document metal concentration, metal resistance and antibiotic resistance along a sediment archive from a pond in the North West of the United Kingdom covering over a century of anthropogenic pollution. We specifically focus on zinc, as it is a ubiquitous and toxic metal contaminant known to co-select for antibiotic resistance, to assess the impact of temporal variation in heavy metal pollution on microbial community diversity and to quantify the selection effects of differential heavy metal exposure on antibiotic resistance. Zinc concentration and bioavailability was found to vary over the core, likely reflecting increased industrialisation around the middle of the 20th century. Zinc concentration had a significant effect on bacterial community composition, as revealed by a positive correlation between the level of zinc tolerance in culturable bacteria and zinc concentration. The proportion of zinc resistant isolates was also positively correlated with resistance to three clinically relevant antibiotics (oxacillin, cefotaxime and trimethoprim). The abundance of the class 1 integron-integrase gene, intI1, marker for anthropogenic pollutants correlated with the prevalence of zinc- and cefotaxime resistance but not with oxacillin and trimethoprim resistance. Our microbial palaeontology approach reveals that metal-contaminated sediments from depths that pre-date the use of antibiotics were enriched in antibiotic resistant bacteria, demonstrating the pervasive effects of metal-antibiotic co-selection in the environment.
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2018
Sierocinski P, Bayer F, Yvon-Durocher G, Burdon M, Großkopf T, Alston M, Swarbreck D, Hobbs PJ, Soyer OS, Buckling A, et al (2018). Biodiversity-function relationships in methanogenic communities.
Mol Ecol,
27(22), 4641-4651.
Abstract:
Biodiversity-function relationships in methanogenic communities.
Methanogenic communities play a crucial role in carbon cycling and biotechnology (anaerobic digestion), but our understanding of how their diversity, or composition in general, determines the rate of methane production is very limited. Studies to date have been correlational because of the difficulty in cultivating their constituent species in pure culture. Here, we investigate the causal link between methanogenesis and diversity in laboratory anaerobic digesters by experimentally manipulating the diversity of cultures by dilution and subsequent equilibration of biomass. This process necessarily leads to the loss of the rarer species from communities. We find a positive relationship between methane production and the number of taxa, with little evidence of functional saturation, suggesting that rare species play an important role in methane-producing communities. No correlations were found between the initial composition and methane production across natural communities, but a positive relationship between species richness and methane production emerged following ecological selection imposed by the laboratory conditions. Our data suggest methanogenic communities show little functional redundancy, and hence, any loss of diversity-both natural and resulting from changes in propagation conditions during anaerobic digestion-is likely to reduce methane production.
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2017
Sierocinski P, Milferstedt K, Bayer F, Großkopf T, Alston M, Bastkowski S, Swarbreck D, Hobbs PJ, Soyer OS, Hamelin J, et al (2017). A Single Community Dominates Structure and Function of a Mixture of Multiple Methanogenic Communities.
Curr Biol,
27(21), 3390-3395.e4.
Abstract:
A Single Community Dominates Structure and Function of a Mixture of Multiple Methanogenic Communities.
The ecology of microbes frequently involves the mixing of entire communities (community coalescence), for example, flooding events, host excretion, and soil tillage [1, 2], yet the consequences of this process for community structure and function are poorly understood [3-7]. Recent theory suggests that a community, due to coevolution between constituent species, may act as a partially cohesive unit [8-11], resulting in one community dominating after community coalescence. This dominant community is predicted to be the one that uses resources most efficiently when grown in isolation [11]. We experimentally tested these predictions using methanogenic communities, for which efficient resource use, quantified by methane production, requires coevolved cross-feeding interactions between species [12]. After propagation in laboratory-scale anaerobic digesters, community composition (determined from 16S rRNA sequencing) and methane production of mixtures of communities closely resembled that of the single most productive community grown in isolation. Analysis of each community's contribution toward the final mixture suggests that certain combinations of taxa within a community might be co-selected as a result of coevolved interactions. As a corollary of these findings, we also show that methane production increased with the number of inoculated communities. These findings are relevant to the understanding of the ecological dynamics of natural microbial communities, as well as demonstrating a simple method of predictably enhancing microbial community function in biotechnology, health, and agriculture [13].
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Sierocinski P, Milferstedt K, Bayer F, Großkopf T, Alston M, Bastkowski S, Swarbreck D, Hobbs PJ, Soyer OS, Hamelin J, et al (2017). Predicting the structure and function of coalesced microbial communities.
Abstract:
Predicting the structure and function of coalesced microbial communities
ABSTRACTMicrobial communities commonly coalesce in nature, but the consequences for resultant community structure and function is unclear. Consistent with recent theory, we demonstrate using methanogenic communities that the most productive communities in isolation dominated when communities were mixed. As a corollary of this dynamic, total methane production increased with the number of inoculated communities. The cohesion and dominance of single communities was explained by more “niche-packed” communities being both more efficient at exploiting resources and resistant to invasion, rather than a function of the average performance of component species. These results are likely to be relevant to the ecological dynamics of natural microbial communities, as well as demonstrating a simple method to predictably enhance microbial community function in biotechnology, health and agriculture.
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2016
Vos M, Mcleman, Buckling, Hesse, Sierocinski, Johnsen PJ, Perron GG, Huelter N (2016). No effect of natural transformation on the evolution of resistance to bacteriophages in the Acinetobacter baylyi model system. Scientific Reports
Friman V-P, Soanes-Brown D, Sierocinski P, Molin S, Johansen HK, Merabishvili M, Pirnay J-P, De Vos D, Buckling A (2016). Pre-adapting parasitic phages to a pathogen leads to increased pathogen clearance and lowered resistance evolution with Pseudomonas aeruginosa cystic fibrosis bacterial isolates.
J Evol Biol,
29(1), 188-198.
Abstract:
Pre-adapting parasitic phages to a pathogen leads to increased pathogen clearance and lowered resistance evolution with Pseudomonas aeruginosa cystic fibrosis bacterial isolates.
Recent years have seen renewed interest in phage therapy--the use of viruses to specifically kill disease-causing bacteria--because of the alarming rise in antibiotic resistance. However, a major limitation of phage therapy is the ease at with bacteria can evolve resistance to phages. Here, we determined whether in vitro experimental coevolution can increase the efficiency of phage therapy by limiting the resistance evolution of intermittent and chronic cystic fibrosis Pseudomonas aeruginosa lung isolates to four different phages. We first pre-adapted all phage strains against all bacterial strains and then compared the efficacy of pre-adapted and nonadapted phages against ancestral bacterial strains. We found that evolved phages were more efficient in reducing bacterial densities than ancestral phages. This was primarily because only 50% of bacterial strains were able to evolve resistance to evolved phages, whereas all bacteria were able to evolve some level of resistance to ancestral phages. Although the rate of resistance evolution did not differ between intermittent and chronic isolates, it incurred a relatively higher growth cost for chronic isolates when measured in the absence of phages. This is likely to explain why evolved phages were more effective in reducing the densities of chronic isolates. Our data show that pathogen genotypes respond differently to phage pre-adaptation, and as a result, phage therapies might need to be individually adjusted for different patients.
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2011
Esser D, Kouril T, Zaparty M, Sierocinski P, Chan PP, Lowe T, Van der Oost J, Albers S-V, Schomburg D, Makarova KS, et al (2011). Functional curation of the Sulfolobus solfataricus P2 and S. acidocaldarius 98-3 complete genome sequences.
Extremophiles,
15(6), 711-712.
Abstract:
Functional curation of the Sulfolobus solfataricus P2 and S. acidocaldarius 98-3 complete genome sequences.
The thermoacidophiles Sulfolobus solfataricus P2 and S. acidocaldarius 98-3 are considered key model organisms representing a major phylum of the Crenarchaeota. Because maintaining current, accurate genome information is indispensable for modern biology, we have updated gene function annotation using the arCOGs database, plus other available functional, structural and phylogenetic information. The goal of this initiative is continuous improvement of genome annotation with the support of the Sulfolobus research community.
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Walther J, Sierocinski P, van der Oost J (2011). Hot transcriptomics.
Archaea,
2010Abstract:
Hot transcriptomics.
DNA microarray technology allows for a quick and easy comparison of complete transcriptomes, resulting in improved molecular insight in fluctuations of gene expression. After emergence of the microarray technology about a decade ago, the technique has now matured and has become routine in many molecular biology laboratories. Numerous studies have been performed that have provided global transcription patterns of many organisms under a wide range of conditions. Initially, implementation of this high-throughput technology has lead to high expectations for ground breaking discoveries. Here an evaluation is performed of the insight that transcriptome analysis has brought about in the field of hyperthermophilic archaea. The examples that will be discussed have been selected on the basis of their impact, in terms of either biological insight or technological progress.
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2010
Zaparty M, Esser D, Gertig S, Haferkamp P, Kouril T, Manica A, Pham TK, Reimann J, Schreiber K, Sierocinski P, et al (2010). "Hot standards" for the thermoacidophilic archaeon Sulfolobus solfataricus.
Extremophiles,
14(1), 119-142.
Abstract:
"Hot standards" for the thermoacidophilic archaeon Sulfolobus solfataricus.
Within the archaea, the thermoacidophilic crenarchaeote Sulfolobus solfataricus has become an important model organism for physiology and biochemistry, comparative and functional genomics, as well as, more recently also for systems biology approaches. Within the Sulfolobus Systems Biology ("SulfoSYS")-project the effect of changing growth temperatures on a metabolic network is investigated at the systems level by integrating genomic, transcriptomic, proteomic, metabolomic and enzymatic information for production of a silicon cell-model. The network under investigation is the central carbohydrate metabolism. The generation of high-quality quantitative data, which is critical for the investigation of biological systems and the successful integration of the different datasets, derived for example from high-throughput approaches (e.g. transcriptome or proteome analyses), requires the application and compliance of uniform standard protocols, e.g. for growth and handling of the organism as well as the "-omics" approaches. Here, we report on the establishment and implementation of standard operating procedures for the different wet-lab and in silico techniques that are applied within the SulfoSYS-project and that we believe can be useful for future projects on Sulfolobus or (hyper)thermophiles in general. Beside established techniques, it includes new methodologies like strain surveillance, the improved identification of membrane proteins and the application of crenarchaeal metabolomics.
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Pham TK, Sierocinski P, van der Oost J, Wright PC (2010). Quantitative proteomic analysis of Sulfolobus solfataricus membrane proteins.
J Proteome Res,
9(2), 1165-1172.
Abstract:
Quantitative proteomic analysis of Sulfolobus solfataricus membrane proteins.
A quantitative proteomic analysis of the membrane of the archaeon Sulfolobus solfataricus P2 using iTRAQ was successfully demonstrated in this technical note. The estimated number of membrane proteins of this organism is 883 (predicted based on Gravy score), corresponding to 30% of the total number of proteins. Using a modified iTRAQ protocol for membrane protein analysis, of the 284 proteins detected, 246 proteins were identified as membrane proteins, while using an original iTRAQ protocol, 147 proteins were detected with only 133 proteins being identified as membrane proteins. Furthermore, 97.2% of proteins identified in the modified protocol contained more than 2 distinct peptides compared to the original workflow. The successful application of this modified protocol offers a potential technique for quantitatively analyzing membrane-associated proteomes of organisms in the archaeal kingdom. The combination of 3 different iTRAQ experiments resulted in the detection of 395 proteins (>or=2 distinct peptides) of which 373 had predicted membrane properties. Approximately 20% of the quantified proteins were observed to exhibit >or=1.5-fold differential expression at temperatures well below the optimum for growth.
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2009
Albers S-V, Birkeland N-K, Driessen AJM, Gertig S, Haferkamp P, Klenk H-P, Kouril T, Manica A, Pham TK, Ruoff P, et al (2009). SulfoSYS (Sulfolobus Systems Biology): towards a silicon cell model for the central carbohydrate metabolism of the archaeon Sulfolobus solfataricus under temperature variation.
Biochem Soc Trans,
37(Pt 1), 58-64.
Abstract:
SulfoSYS (Sulfolobus Systems Biology): towards a silicon cell model for the central carbohydrate metabolism of the archaeon Sulfolobus solfataricus under temperature variation.
SulfoSYS (Sulfolobus Systems Biology) focuses on the study of the CCM (central carbohydrate metabolism) of Sulfolobus solfataricus and its regulation under temperature variation at the systems level. In Archaea, carbohydrates are metabolized by modifications of the classical pathways known from Bacteria or Eukarya, e.g. the unusual branched ED (Entner-Doudoroff) pathway, which is utilized for glucose degradation in S. solfataricus. This archaeal model organism of choice is a thermoacidophilic crenarchaeon that optimally grows at 80 degrees C (60-92 degrees C) and pH 2-4. In general, life at high temperature requires very efficient adaptation to temperature changes, which is most difficult to deal with for organisms, and it is unclear how biological networks can withstand and respond to such changes. This integrative project combines genomic, transcriptomic, proteomic and metabolomic, as well as kinetic and biochemical information. The final goal of SulfoSYS is the construction of a silicon cell model for this part of the living cell that will enable computation of the CCM network. In the present paper, we report on one of the first archaeal systems biology projects.
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