School of Agriculture, Food and Ecosystem Sciences - Research Publications
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ItemProtistan predation selects for antibiotic resistance in soil bacterial communities(Oxford University Press, 2023-12)Understanding how antibiotic resistance emerges and evolves in natural habitats is critical for predicting and mitigating antibiotic resistance in the context of global change. Bacteria have evolved antibiotic production as a strategy to fight competitors, predators and other stressors, but how predation pressure of their most important consumers (i.e., protists) affects soil antibiotic resistance genes (ARGs) profiles is still poorly understood. To address this gap, we investigated responses of soil resistome to varying levels of protistan predation by inoculating low, medium and high concentrations of indigenous soil protist suspensions in soil microcosms. We found that an increase in protistan predation pressure was strongly associated with higher abundance and diversity of soil ARGs. High protist concentrations significantly enhanced the abundances of ARGs encoding multidrug (oprJ and ttgB genes) and tetracycline (tetV) efflux pump by 608%, 724% and 3052%, respectively. Additionally, we observed an increase in the abundance of numerous bacterial genera under high protistan pressure. Our findings provide empirical evidence that protistan predation significantly promotes antibiotic resistance in soil bacterial communities and advances our understanding of the biological driving forces behind the evolution and development of environmental antibiotic resistance.
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ItemNo Preview AvailableTrophic interrelationships of bacteria are important for shaping soil protist communities(WILEY, 2023-08)Protists occupy multiple trophic positions in soil food webs and significantly contribute to organic matter decomposition and biogeochemical cycling. Protists can ingest bacteria and fungi as main food sources while being subjected to predation of invertebrates, but our understanding of how bottom-up and top-down regulations structure protists in natural soil habitats is limited. Here, we disentangle the effects of trophic regulations to the diversity and structure of soil protists in natural settings across northern and eastern Australia. Bacterial and invertebrate diversity were identified as important drivers of the diversity of functional groups of protists. Moreover, the compositions of protistan taxonomic and functional groups were better predicted by bacteria and fungi, than by soil invertebrates. There were strong trophic interconnections between protists and bacteria in multiple organismic network analysis. Altogether, the study provided new evidence that, bottom-up control of bacteria played an important role in shaping the soil protist community structure, which can be derived from feeding preferences of protists on microbial prey, and their intimate relationships in soil functioning or environmental adaptation. Our findings advance our knowledge about the impacts of different trophic groups on key soil organismic communities, with implications for ecosystem functions and services.
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ItemNo Preview AvailableLivestock manure spiked with the antibiotic tylosin significantly altered soil protist functional groups(ELSEVIER, 2022-04-05)With the increasing global antibiotic uses in livestock husbandry, animal manures upon land application pose potential threats to the environments and soil microbiome. Nevertheless, effects of manures and antibiotic-administered manures on soil protists, an integral component of soil food web and primary regulators of bacteria, remain unknown. Here, we assessed impacts of cattle and poultry manures with or without an antibiotic tylosin on soil protists and their functional groups in a 130-day microcosm incubation. Protists were highly responsive to manure application, with a significant decline in their alpha diversity in all manure treatments. There were also significant temporal changes in the alpha diversity and composition of soil protists and their functional groups. Poultry manures had stronger negative influences on the community structure of protists compared to cattle manures, and more pronounced effects on protists were observed in tylosin-spiked manure treatments. Furthermore, many consumer, phototrophic and parasitic taxa were highly susceptible to all manure treatments at Day 50 and 130. Altogether, our findings demonstrate negative effects of animal manures and tylosin on soil protists. This study suggests that the applications of livestock manures and antibiotics may subsequently alter ecological functions of protists and their interactions with other soil microorganisms in agricultural systems.
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ItemNo Preview AvailableContrasting ecological processes shape the Eucalyptus phyllosphere bacterial and fungal community assemblies(Wiley, 2022-03-01)Abstract Introduction Phyllosphere microbiome is intrinsically linked to plant performance and ecosystem functioning. However, our knowledge about the role of ecological processes in shaping the biogeography of different phyllosphere microbial communities is scarce. Materials and Methods Here, we compared the biogeographic patterns of bacterial and fungal communities in phyllosphere samples of plants belonging to the genus of Eucalyptus of the Myrtaceae family collected from an over 4000 km transect. We investigated the relative importance of two major ecosystem processes (stochastic vs. deterministic) in shaping phyllosphere microbial community assemblies. Results Our results demonstrated that the neutral community model, which can quantify the degree of a community assembly determined by stochastic processes, explained 64.2% of the variations in bacterial community assembly, which had a normalized stochasticity ratio of 71.8%. These results suggest that the dominant role of stochastic processes in shaping bacterial community assembly. In contrast, phyllosphere fungal community assembly was mainly shaped by deterministic processes as revealed by a relatively small explanation rate of the neutral community model (48.7%) and a normalized stochasticity ratio of 25.1%. Variation partitioning analysis and random forest modelling results indicated that climatic factors, particularly mean annual precipitation and aridity index, were important in driving both bacterial and fungal biogeographic patterns in the phyllosphere. Edaphic factors, such as soil organic and mineral nitrogen content, were more closely related to fungal community assembly than to bacterial community assembly. The differential responses of bacterial and fungal communities to environmental factors could be attributed to the different traits of bacteria and fungi, that is, the higher potential dispersal rate and wider habitat niche of bacteria than fungi. Conclusion Our findings demonstrated that phyllosphere bacterial and fungal communities followed distinct community assembly processes, which is supported by the ‘size plasticity’ hypothesis that smaller organisms (bacteria) are less influenced by environmental conditions and are more homogeneous across space than larger organisms (fungi). These findings provide new insights into the microbial ecology of plant phyllosphere microbiomes.
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ItemMicrobial regulation of natural antibiotic resistance: Understanding the protist-bacteria interactions for evolution of soil resistome(Elsevier BV, 2020-02-25)The emergence, evolution and spread of antibiotic resistance genes (ARGs) in the environment represent a global threat to human health. Our knowledge of antibiotic resistance in human-impacted ecosystems is rapidly growing with antibiotic use, organic fertilization and wastewater irrigation identified as key selection pressures. However, the importance of biological interactions, especially predation and competition, as a potential driver of antibiotic resistance in the natural environment with limited anthropogenic disturbance remains largely overlooked. Stress-affected bacteria develop resistance to maximize competition and survival, and similarly bacteria may develop resistance to fight stress under the predation pressure of protists, an essential component of the soil microbiome. In this article, we summarized the major findings for the prevalence of natural ARGs on our planet and discussed the potential selection pressures driving the evolution and development of antibiotic resistance in natural settings. This is the first article that reviewed the potential links between protists and the antibiotic resistance of bacteria, and highlighted the importance of predation by protists as a crucial selection pressure of antibiotic resistance in the absence of anthropogenic disturbance. We conclude that an improved ecological understanding of the protists-bacteria interactions and other biological relationships would greatly expand our ability to predict and mitigate the environmental antibiotic resistance under the context of global change.
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ItemOxytetracycline and Ciprofloxacin Exposure Altered the Composition of Protistan Consumers in an Agricultural Soil(AMER CHEMICAL SOC, 2020-08-04)Protists, an integral component of soil microbiome, are one of the main predators of bacteria. Bacteria can produce toxic secondary metabolites, e.g., antibiotics to fight stress under the predation pressure of protists; however, impacts of antibiotics on the profile of protists in soils remain unclear. Here, we constructed a microcosm incubation to investigate the effects of two common antibiotics, oxytetracycline and ciprofloxacin, on the protistan and bacterial communities in an arable soil. Rhizaria were the most abundant protist supergroup, followed by Amoebozoa, Stramenopiles, and Aveolata. Among trophic functional groups, consumers were predominant within the protistan community. The protistan alpha-diversity was not significantly changed, while the bacterial alpha-diversity was decreased under the pressure of antibiotics. Nevertheless, the antibiotic exposure considerably reduced the relative abundance of protistan lineages in Rhizaria and Amoebozoa, which were the dominant supergroups of protistan consumers, while increased the relative abundance of other consumer and phototrophic protists. Altogether, we provide novel experimental evidence that the bacterivorous consumers, an important functional group of protists, were more sensitive to antibiotics than other functional groups. Our findings have potential implications for the induced alterations of protistan community and their ecological functions under the scenarios of projected increasing global antibiotic usage.
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ItemDeterministic selection dominates microbial community assembly in termite mounds(Elsevier, 2021-01-01)Termite mounds are an important habitat for an enormous diversity of microorganisms. However, the microbial community assembly processes in termite mounds remain unresolved, which impeded our ability to predict the biological functions of these mound-associated microbiota under the global changes. Here we conducted a large-scale investigation in northern Australia to explore biogeographical patterns of microbial community in termite mounds and identify the role of deterministic and stochastic processes in microbial community assembly. Microbial communities in termite mounds exhibited a significant distance-decay pattern, and fungi had a stronger distance-decay relationship than bacteria. The neutral community model and normalized stochasticity ratio index (NST) revealed that the deterministic selection, rather than stochastic forces, predominated the microbial community assembly in termite mounds. Deterministic processes exhibited a significantly weaker impact on bacteria (NST = 45.23%) than on fungi (NST = 33.72%), likely due to the wider habitat niche breadth and higher potential migration rate of bacteria. Random forest model further demonstrated that mean annual temperature was the most important predictor of both bacterial and fungal profiles in termite mounds. These findings improved our understanding of spatial patterns and processes of microbiome in termite mounds, which is critical to decipher the role of termite mounds associated microbes in regulating ecosystem multifunctionality.
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ItemNo Preview AvailableNiche specialization of comammox Nitrospira clade A in terrestrial ecosystems(PERGAMON-ELSEVIER SCIENCE LTD, 2021-05)Comammox Nitrospira are a newly discovered group of nitrifying prokaryotes and might be key contributors to nitrogen cycling in terrestrial ecosystems. Their large-scale distribution patterns and the dominant environmental factors shaping their ecological niches are not yet well documented. Here, we investigated the biogeographic distribution of comammox Nitrospira over 4000 km in eastern Australia and explored the niche specialization of individual comammox Nitrospira phylotypes. Our results revealed that the abundance, richness and community composition of comammox Nitrospira clade A were best predicted by mean annual precipitation (MAP) among all the determined environmental parameters. We identified four phylogenetic clusters of comammox Nitrospira: clade A.1, A.2.1, A.2.2 and A.3. MAP was consistently the strongest factor correlated with the relative abundances of the dominant clades, A.2.1 and A.3. MAP and other variables including soil nitrate, mean annual temperature and total nitrogen showed contrasting effects on the relative abundances of comammox Nitrospira clade A.2.1 and A.3, indicating their potential ecological niche differentiation in the soils. Together, we found a broad distribution of comammox Nitrospira clade A, but not clade B, in various terrestrial ecosystems across eastern Australia, and the abundance and diversity of comammox Nitrospira clade A can be mainly predicted by MAP among all the determined environmental parameters. These findings provide novel evidence for the environmental adaptation and niche specialization of comammox Nitrospira in the terrestrial ecosystems.
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ItemTermite mounds reduce soil microbial diversity by filtering rare microbial taxa.(Wiley, 2021-04-05)Termites are ubiquitous insects in tropical and subtropical habitats, and some of them construct massive nests ('mounds'), which substantially promote substrate heterogeneity by altering soil properties. Yet, the role of termite nesting process in regulating the distribution and diversity of soil microbial communities remains poorly understood, which introduces uncertainty in predictions of ecosystem functions of termite mounds in a changing environment. Here, by using amplicon sequencing, we conducted a survey of 134 termite mounds across >1500 km in northern Australia and found that termite mounds significantly differed from bulk soils in the microbial diversity and community compositions. Compared with bulk soils, termite nesting process decreased the microbial diversity and the relative abundance of rare taxa. Rare taxa had a narrower habitat niche breadth than dominant taxa and might be easier to be filtered by the potential intensive microbial competition during the nesting processes. We further demonstrated that the shift in pH induced by termite nesting process was a major driver shaping the microbial community profiles in termite mounds. Together, our work provides novel evidence that termite nesting is an important process in regulating soil microbial diversity, which advances our understanding of the functioning of termite mounds.
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ItemBiotic and abiotic factors distinctly drive contrasting biogeographic patterns between phyllosphere and soil resistomes in natural ecosystems(Springer Science and Business Media LLC, 2021-12)The phyllosphere and soil are two of the most important reservoirs of antibiotic resistance genes (ARGs) in terrestrial ecosystems. However, comparative studies on the biogeographic patterns of ARGs in these two habitats are lacking. Based on the construction of ARG abundance atlas across a > 4,000 km transect in eastern and northern Australia, we found contrasting biogeographic patterns of the phyllosphere and soil resistomes, which showed their distinct responses to the biotic and abiotic stresses. The similarity of ARG compositions in soil, but not in the phyllosphere, exhibited significant distance-decay patterns. ARG abundance in the phyllosphere was mainly correlated with the compositions of co-occurring bacterial, fungal and protistan communities, indicating that biotic stresses were the main drivers shaping the phyllosphere resistome. Soil ARG abundance was mainly associated with abiotic factors including mean annual temperature and precipitation as well as soil total carbon and nitrogen. Our findings demonstrated the distinct roles of biotic and abiotic factors in shaping resistomes in different environmental habitats. These findings constitute a major advance in our understanding of the current environmental resistomes and contribute to better predictions of the evolution of environmental ARGs by highlighting the importance of habitat difference in shaping environmental resistomes.