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1.
mBio ; 15(5): e0001224, 2024 May 08.
Artigo em Inglês | MEDLINE | ID: mdl-38634692

RESUMO

The microbiome expresses a variety of functions that influence host biology. The range of functions depends on the microbiome's composition, which can change during the host's lifetime due to neutral assembly processes, host-mediated selection, and environmental conditions. To date, the exact dynamics of microbiome assembly, the underlying determinants, and the effects on host-associated functions remain poorly understood. Here, we used the nematode Caenorhabditis elegans and a defined community of fully sequenced, naturally associated bacteria to study microbiome dynamics and functions across a major part of the worm's lifetime of hosts under controlled experimental conditions. Bacterial community composition initially shows strongly declining levels of stochasticity, which increases during later time points, suggesting selective effects in younger animals as opposed to more random processes in older animals. The adult microbiome is enriched in genera Ochrobactrum and Enterobacter compared to the direct substrate and a host-free control environment. Using pathway analysis, metabolic, and ecological modeling, we further find that the lifetime assembly dynamics increase competitive strategies and gut-associated functions in the host-associated microbiome, indicating that the colonizing bacteria benefit the worm. Overall, our study introduces a framework for studying microbiome assembly dynamics based on stochastic, ecological, and metabolic models, yielding new insights into the processes that determine host-associated microbiome composition and function. IMPORTANCE: The microbiome plays a crucial role in host biology. Its functions depend on the microbiome composition that can change during a host's lifetime. To date, the dynamics of microbiome assembly and the resulting functions still need to be better understood. This study introduces a new approach to characterize the functional consequences of microbiome assembly by modeling both the relevance of stochastic processes and metabolic characteristics of microbial community changes. The approach was applied to experimental time-series data obtained for the microbiome of the nematode Caenorhabditis elegans across the major part of its lifetime. Stochastic processes played a minor role, whereas beneficial bacteria as well as gut-associated functions enriched in hosts. This indicates that the host might actively shape the composition of its microbiome. Overall, this study provides a framework for studying microbiome assembly dynamics and yields new insights into C. elegans microbiome functions.


Assuntos
Bactérias , Caenorhabditis elegans , Microbioma Gastrointestinal , Animais , Caenorhabditis elegans/microbiologia , Caenorhabditis elegans/fisiologia , Microbioma Gastrointestinal/fisiologia , Bactérias/classificação , Bactérias/genética , Bactérias/isolamento & purificação , Interações entre Hospedeiro e Microrganismos , Trato Gastrointestinal/microbiologia , Microbiota
2.
Front Microbiol ; 15: 1347422, 2024.
Artigo em Inglês | MEDLINE | ID: mdl-38476944

RESUMO

Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven classical and emerging multicellular model organisms across the phylogenetic tree of life. To determine the microbial community composition of each host, we utilized a combination of archaea and bacteria-specific 16S rRNA gene amplicons. Members of the two prokaryotic domains were described regarding their community composition, diversity, and richness in each multicellular host. Moreover, association with specific hosts and possible interaction partners between the bacterial and archaeal communities were determined for the marine models. Our data show that the archaeome in marine hosts predominantly consists of Nitrosopumilaceae and Nanoarchaeota, which represent keystone taxa among the porifera. The presence of an archaeome in the terrestrial hosts varies substantially. With respect to abundant archaeal taxa, they harbor a higher proportion of methanoarchaea over the aquatic environment. We find that the archaeal community is much less diverse than its bacterial counterpart. Archaeal amplicon sequence variants are usually host-specific, suggesting adaptation through co-evolution with the host. While bacterial richness was higher in the aquatic than the terrestrial hosts, a significant difference in diversity and richness between these groups could not be observed in the archaeal dataset. Our data show a large proportion of unclassifiable archaeal taxa, highlighting the need for improved cultivation efforts and expanded databases.

3.
Microbiol Spectr ; 12(2): e0114423, 2024 Feb 06.
Artigo em Inglês | MEDLINE | ID: mdl-38230938

RESUMO

While numerous health-beneficial interactions between host and microbiota have been identified, there is still a lack of targeted approaches for modulating these interactions. Thus, we here identify precision prebiotics that specifically modulate the abundance of a microbiome member species of interest. In the first step, we show that defining precision prebiotics by compounds that are only taken up by the target species but no other species in a community is usually not possible due to overlapping metabolic niches. Subsequently, we use metabolic modeling to identify precision prebiotics for a two-member Caenorhabditis elegans microbiome community comprising the immune-protective target species Pseudomonas lurida MYb11 and the persistent colonizer Ochrobactrum vermis MYb71. We experimentally confirm four of the predicted precision prebiotics, L-serine, L-threonine, D-mannitol, and γ-aminobutyric acid, to specifically increase the abundance of MYb11. L-serine was further assessed in vivo, leading to an increase in MYb11 abundance also in the worm host. Overall, our findings demonstrate that metabolic modeling is an effective tool for the design of precision prebiotics as an important cornerstone for future microbiome-targeted therapies.IMPORTANCEWhile various mechanisms through which the microbiome influences disease processes in the host have been identified, there are still only few approaches that allow for targeted manipulation of microbiome composition as a first step toward microbiome-based therapies. Here, we propose the concept of precision prebiotics that allow to boost the abundance of already resident health-beneficial microbial species in a microbiome. We present a constraint-based modeling pipeline to predict precision prebiotics for a minimal microbial community in the worm Caenorhabditis elegans comprising the host-beneficial Pseudomonas lurida MYb11 and the persistent colonizer Ochrobactrum vermis MYb71 with the aim to boost the growth of MYb11. Experimentally testing four of the predicted precision prebiotics, we confirm that they are specifically able to increase the abundance of MYb11 in vitro and in vivo. These results demonstrate that constraint-based modeling could be an important tool for the development of targeted microbiome-based therapies against human diseases.


Assuntos
Microbiota , Prebióticos , Pseudomonas , Animais , Humanos , Caenorhabditis elegans , Serina
4.
Proc Biol Sci ; 290(2012): 20232193, 2023 Dec 06.
Artigo em Inglês | MEDLINE | ID: mdl-38052248

RESUMO

The microbiota shapes host biology in numerous ways. One example is protection against pathogens, which is likely critical for host fitness in consideration of the ubiquity of pathogens. The host itself can affect abundance of microbiota or pathogens, which has usually been characterized in separate studies. To date, however, it is unclear how the host influences the interaction with both simultaneously and how this triangular interaction determines fitness of the host-microbe assemblage, the so-called metaorganism. To address this current knowledge gap, we focused on a triangular model interaction, consisting of the nematode Caenorhabditis elegans, its protective symbiont Pseudomonas lurida MYb11 and its pathogen Bacillus thuringiensis Bt679. We combined the two microbes with C. elegans mutants with altered immunity and/or microbial colonization, and found that (i) under pathogen stress, immunocompetence has a larger influence on metaorganism fitness than colonization with the protective microbe; (ii) in almost all cases, MYb11 still improves fitness; and (iii) disruption of p38 MAPK signalling, which contributes centrally to immunity against Bt679, completely reverses the protective effect of MYb11, which further reduces nematode survival and fitness upon infection with Bt679. Our study highlights the complex interplay between host, protective microbe and pathogen in shaping metaorganism biology.


Assuntos
Bacillus thuringiensis , Proteínas de Caenorhabditis elegans , Microbiota , Animais , Caenorhabditis elegans
5.
ISME J ; 17(11): 1953-1965, 2023 11.
Artigo em Inglês | MEDLINE | ID: mdl-37673969

RESUMO

Most animals and plants have associated microorganisms, collectively referred to as their microbiomes, which can provide essential functions. Given their importance, host-associated microbiomes have the potential to contribute substantially to adaptation of the host-microbiome assemblage (the "metaorganism"). Microbiomes may be especially important for rapid adaptation to novel environments because microbiomes can change more rapidly than host genomes. However, it is not well understood how hosts and microbiomes jointly contribute to metaorganism adaptation. We developed a model system with which to disentangle the contributions of hosts and microbiomes to metaorganism adaptation. We established replicate mesocosms containing the nematode Caenorhabditis elegans co-cultured with microorganisms in a novel complex environment (laboratory compost). After approximately 30 nematode generations (100 days), we harvested worm populations and associated microbiomes, and subjected them to a common garden experiment designed to unravel the impacts of microbiome composition and host genetics on metaorganism adaptation. We observed that adaptation took different trajectories in different mesocosm lines, with some increasing in fitness and others decreasing, and that interactions between host and microbiome played an important role in these contrasting evolutionary paths. We chose two exemplary mesocosms (one with a fitness increase and one with a decrease) for detailed study. For each example, we identified specific changes in both microbiome composition (for both bacteria and fungi) and nematode gene expression associated with each change in fitness. Our study provides experimental evidence that adaptation to a novel environment can be jointly influenced by host and microbiome.


Assuntos
Microbiota , Animais , Evolução Biológica , Genoma , Bactérias/genética
6.
bioRxiv ; 2023 Feb 18.
Artigo em Inglês | MEDLINE | ID: mdl-36824941

RESUMO

The microbiome is increasingly receiving attention as an important modulator of host health and disease. However, while numerous mechanisms through which the microbiome influences its host have been identified, there is still a lack of approaches that allow to specifically modulate the abundance of individual microbes or microbial functions of interest. Moreover, current approaches for microbiome manipulation such as fecal transfers often entail a non-specific transfer of entire microbial communities with potentially unwanted side effects. To overcome this limitation, we here propose the concept of precision prebiotics that specifically modulate the abundance of a microbiome member species of interest. In a first step, we show that defining precision prebiotics by compounds that are only taken up by the target species but no other species in a community is usually not possible due to overlapping metabolic niches. Subsequently, we present a metabolic modeling network framework that allows us to define precision prebiotics for a two-member C. elegans microbiome model community comprising the immune-protective Pseudomonas lurida MYb11 and the persistent colonizer Ochrobactrum vermis MYb71. Thus, we predicted compounds that specifically boost the abundance of the host-beneficial MYb11, four of which were experimentally validated in vitro (L-serine, L-threonine, D-mannitol, and γ-aminobutyric acid). L-serine was further assessed in vivo, leading to an increase in MYb11 abundance also in the worm host. Overall, our findings demonstrate that constraint-based metabolic modeling is an effective tool for the design of precision prebiotics as an important cornerstone for future microbiome-targeted therapies.

7.
J Vis Exp ; (186)2022 08 17.
Artigo em Inglês | MEDLINE | ID: mdl-36063004

RESUMO

The nematode Caenorhabditis elegans interacts with a large diversity of microorganisms in nature. In general, C. elegans is commonly found in rotten plant matter, especially rotten fruits like apples or on compost heaps. It is also associated with certain invertebrate hosts such as slugs and woodlice. These habitats are rich in microbes, which serve as food for C. elegans and which can also persistently colonize the nematode gut. To date, the exact diversity and consistency of the native C. elegans microbiota across habitats and geographic locations is not fully understood. Here, we describe a suitable approach for isolating C. elegans from nature and characterizing the microbiota of worms. Nematodes can be easily isolated from compost material, rotting apples, slugs, or attracted by placing apples on compost heaps. The prime time for finding C. elegans in the Northern Hemisphere is from September until November. Worms can be washed out of collected substrate material by immersing the substrate in buffer solution, followed by the collection of nematodes and their transfer onto nematode growth medium or PCR buffer for subsequent analysis. We further illustrate how the samples can be used to isolate and purify the worm-associated microorganisms and to process worms for 16S ribosomal RNA analysis of microbiota community composition. Overall, the described methods may stimulate new research on the characterization of the C. elegans microbiota across habitats and geographic locations, thereby helping to obtain a comprehensive understanding of the diversity and stability of the nematode's microbiota as a basis for future functional research.


Assuntos
Malus , Microbiota , Animais , Caenorhabditis elegans/genética , Frutas , Malus/genética , RNA Ribossômico 16S/genética
8.
Environ Microbiol ; 23(11): 6721-6733, 2021 11.
Artigo em Inglês | MEDLINE | ID: mdl-34414649

RESUMO

Research on the Caenorhabditis elegans microbiota only recently started, with little known about how C. elegans acquires its microbiota. Slugs live in the same habitat as C. elegans and are known vectors for the worm. Hence, we wondered how the passage through a slug affects the C. elegans gut microbiota and whether worms can acquire bacteria from the slug. Using fluorescently labelled microbiota and 16S rRNA gene amplicon sequencing, we evaluated microbiota persistence and acquisition in C. elegans after slug passage. We compared C. elegans gut microbiomes isolated from wild-caught slugs to the microbiomes of worms after experimental slug passage to compare similarities and differences in microbiome composition. We found that microbiota persists in C. elegans while passing the slug gut and that worms simultaneously acquire additional bacteria species from the slug. Although the amplicon sequencing variant (ASV) richness of worms from the experiment did not exceed the richness of worms that naturally occur in slugs, we found a high number of shared ASVs indicating the importance of commonly associated microbiota. We demonstrate that C. elegans can take advantage of its passage through the slug by acquiring new potential microbiota without losing its native microbiota.


Assuntos
Microbioma Gastrointestinal , Gastrópodes , Microbiota , Animais , Caenorhabditis elegans/microbiologia , Gastrópodes/genética , Microbiota/genética , RNA Ribossômico 16S/genética
9.
PLoS Pathog ; 17(4): e1009454, 2021 04.
Artigo em Inglês | MEDLINE | ID: mdl-33793670

RESUMO

In C. elegans, 283 clec genes encode a highly diverse family of C-type lectin-like domain (CTLD) proteins. Since vertebrate CTLD proteins have characterized functions in defense responses against pathogens and since expression of C. elegans clec genes is pathogen-dependent, it is generally assumed that clec genes function in C. elegans immune defenses. However, little is known about the relative contribution and exact function of CLEC proteins in C. elegans immunity. Here, we focused on the C. elegans clec gene clec-4, whose expression is highly upregulated by pathogen infection, and its paralogs clec-41 and clec-42. We found that, while mutation of clec-4 resulted in enhanced resistance to the Gram-positive pathogen Bacillus thuringiensis MYBt18247 (Bt247), inactivation of clec-41 and clec-42 by RNAi enhanced susceptibility to Bt247. Further analyses revealed that enhanced resistance of clec-4 mutants to Bt247 was due to an increase in feeding cessation on the pathogen and consequently a decrease in pathogen load. Moreover, clec-4 mutants exhibited feeding deficits also on non-pathogenic bacteria that were in part reflected in the clec-4 gene expression profile, which overlapped with gene sets affected by starvation or mutation in nutrient sensing pathways. However, loss of CLEC-4 function only mildly affected life-history traits such as fertility, indicating that clec-4 mutants are not subjected to dietary restriction. While CLEC-4 function appears to be associated with the regulation of feeding behavior, we show that CLEC-41 and CLEC-42 proteins likely function as bona fide immune effector proteins that have bacterial binding and antimicrobial capacities. Together, our results exemplify functional diversification within clec gene paralogs.


Assuntos
Bacillus thuringiensis/fisiologia , Proteínas de Caenorhabditis elegans/metabolismo , Caenorhabditis elegans/genética , Lectinas Tipo C/metabolismo , Transcriptoma , Animais , Caenorhabditis elegans/imunologia , Caenorhabditis elegans/microbiologia , Proteínas de Caenorhabditis elegans/genética , Comportamento Alimentar , Imunidade , Lectinas Tipo C/genética , Mutação com Perda de Função , Domínios Proteicos , Interferência de RNA , Regulação para Cima
10.
Front Cell Infect Microbiol ; 11: 775634, 2021.
Artigo em Inglês | MEDLINE | ID: mdl-34976859

RESUMO

In comparison with the standard monoxenic maintenance in the laboratory, rearing the nematode Caenorhabditis elegans on its natural microbiota improves its fitness and immunity against pathogens. Although C. elegans is known to exhibit choice behavior and pathogen avoidance behavior, little is known about whether C. elegans actively chooses its (beneficial) microbiota and whether the microbiota influences worm behavior. We examined eleven natural C. elegans isolates in a multiple-choice experiment for their choice behavior toward four natural microbiota bacteria and found that microbiota choice varied among C. elegans isolates. The natural C. elegans isolate MY2079 changed its choice behavior toward microbiota isolate Ochrobactrum vermis MYb71 in both multiple-choice and binary-choice experiments, in particular on proliferating bacteria: O. vermis MYb71 was chosen less than other microbiota bacteria or OP50, but only after preconditioning with MYb71. Examining escape behavior and worm fitness on MYb71, we ruled out pathogenicity of MYb71 and consequently learned pathogen avoidance behavior as the main driver of the behavioral change toward MYb71. The change in behavior of C. elegans MY2079 toward microbiota bacterium MYb71 demonstrates how the microbiota influences the worm's choice. These results might give a baseline for future research on host-microbiota interaction in the C. elegans model.


Assuntos
Microbiota , Ochrobactrum , Animais , Bactérias , Caenorhabditis elegans , Virulência
11.
ISME J ; 14(1): 26-38, 2020 01.
Artigo em Inglês | MEDLINE | ID: mdl-31484996

RESUMO

The microbiota is generally assumed to have a substantial influence on the biology of multicellular organisms. The exact functional contributions of the microbes are often unclear and cannot be inferred easily from 16S rRNA genotyping, which is commonly used for taxonomic characterization of bacterial associates. In order to bridge this knowledge gap, we here analyzed the metabolic competences of the native microbiota of the model nematode Caenorhabditis elegans. We integrated whole-genome sequences of 77 bacterial microbiota members with metabolic modeling and experimental characterization of bacterial physiology. We found that, as a community, the microbiota can synthesize all essential nutrients for C. elegans. Both metabolic models and experimental analyses revealed that nutrient context can influence how bacteria interact within the microbiota. We identified key bacterial traits that are likely to influence the microbe's ability to colonize C. elegans (i.e., the ability of bacteria for pyruvate fermentation to acetoin) and affect nematode fitness (i.e., bacterial competence for hydroxyproline degradation). Considering that the microbiota is usually neglected in C. elegans research, the resource presented here will help our understanding of this nematode's biology in a more natural context. Our integrative approach moreover provides a novel, general framework to characterize microbiota-mediated functions.


Assuntos
Bactérias/metabolismo , Caenorhabditis elegans/microbiologia , Microbiota , Animais , Bactérias/genética , Bactérias/isolamento & purificação , Caenorhabditis elegans/metabolismo , Redes e Vias Metabólicas/genética
12.
Front Microbiol ; 10: 1793, 2019.
Artigo em Inglês | MEDLINE | ID: mdl-31440221

RESUMO

The biology of all organisms is influenced by the associated community of microorganisms. In spite of its importance, it is usually not well understood how exactly this microbiota affects host functions and what are the underlying molecular processes. To rectify this knowledge gap, we took advantage of the nematode Caenorhabditis elegans as a tractable, experimental model system and assessed the inducible transcriptome response after colonization with members of its native microbiota. For this study, we focused on two isolates of the genus Ochrobactrum. These bacteria are known to be abundant in the nematode's microbiota and are capable of colonizing and persisting in the nematode gut, even under stressful conditions. The transcriptome response was assessed across development and three time points of adult life, using general and C. elegans-specific enrichment analyses to identify affected functions. Our assessment revealed an influence of the microbiota members on the nematode's dietary response, development, fertility, immunity, and energy metabolism. This response is mainly regulated by a GATA transcription factor, most likely ELT-2, as indicated by the enrichment of (i) the GATA motif in the promoter regions of inducible genes and (ii) of ELT-2 targets among the differentially expressed genes. We compared our transcriptome results with a corresponding previously characterized proteome data set, highlighting a significant overlap in the differentially expressed genes, the affected functions, and ELT-2 target genes. Our analysis further identified a core set of 86 genes that consistently responded to the microbiota members across development and adult life, including several C-type lectin-like genes and genes known to be involved in energy metabolism or fertility. We additionally assessed the consequences of induced gene expression with the help of metabolic network model analysis, using a previously established metabolic network for C. elegans. This analysis complemented the enrichment analyses by revealing an influence of the Ochrobactrum isolates on C. elegans energy metabolism and furthermore metabolism of specific amino acids, fatty acids, and also folate biosynthesis. Our findings highlight the multifaceted impact of naturally colonizing microbiota isolates on C. elegans life history and thereby provide a framework for further analysis of microbiota-mediated host functions.

13.
BMC Biol ; 17(1): 24, 2019 03 12.
Artigo em Inglês | MEDLINE | ID: mdl-30866929

RESUMO

BACKGROUND: The nematode Caenorhabditis elegans has been extensively used to explore the relationships between complex traits, genotypes, and environments. Complex traits can vary across different genotypes of a species, and the genetic regulators of trait variation can be mapped on the genome using quantitative trait locus (QTL) analysis of recombinant inbred lines (RILs) derived from genetically and phenotypically divergent parents. Most RILs have been derived from crossing two parents from globally distant locations. However, the genetic diversity between local C. elegans populations can be as diverse as between global populations and could thus provide means of identifying genetic variation associated with complex traits relevant on a broader scale. RESULTS: To investigate the effect of local genetic variation on heritable traits, we developed a new RIL population derived from 4 parental wild isolates collected from 2 closely located sites in France: Orsay and Santeuil. We crossed these 4 genetically diverse parental isolates to generate a population of 200 multi-parental RILs and used RNA-seq to obtain sequence polymorphisms identifying almost 9000 SNPs variable between the 4 genotypes with an average spacing of 11 kb, doubling the mapping resolution relative to currently available RIL panels for many loci. The SNPs were used to construct a genetic map to facilitate QTL analysis. We measured life history traits such as lifespan, stress resistance, developmental speed, and population growth in different environments, and found substantial variation for most traits. We detected multiple QTLs for most traits, including novel QTLs not found in previous QTL analysis, including those for lifespan and pathogen responses. This shows that recombining genetic variation across C. elegans populations that are in geographical close proximity provides ample variation for QTL mapping. CONCLUSION: Taken together, we show that using more parents than the classical two parental genotypes to construct a RIL population facilitates the detection of QTLs and that the use of wild isolates facilitates the detection of QTLs. The use of multi-parent RIL populations can further enhance our understanding of local adaptation and life history trade-offs.


Assuntos
Caenorhabditis elegans/genética , Características de História de Vida , Locos de Características Quantitativas , Animais , Mapeamento Cromossômico , Ligação Genética , Genótipo , Organismos Geneticamente Modificados
14.
Proteomics ; 18(8): e1700426, 2018 04.
Artigo em Inglês | MEDLINE | ID: mdl-29513928

RESUMO

The nematode Caenorhabditis elegans interacts with a variety of bacteria as it feeds on microbes, and a number of these both associate and persist within the worm's intestine. Host-microbe interactions in C. elegans have been analyzed primarily at the transcriptome level with the host response often been monitored after challenge with pathogens. We assessed the proteome of C. elegans after growth on bacteria capable of colonizing its gut, via a comparative analysis of the nematode exposed to two naturally associated Ochrobactrum spp. (MYb71, MYb237) versus C. elegans grown on Escherichia coli OP50. A total of 4677 C. elegans proteins were identified, 3941 quantified. Significant alterations in protein abundances were observed for 122 proteins, 48 higher and 74 lower in abundance. We observed an increase in abundance of proteins potentially regulated via host signaling pathways, in addition to proteins involved in processing of foreign entities (e.g., lipase, proteases, glutathione metabolism). Decreased in abundance were proteins involved in both degradation and biosynthesis of amino acids, and enzymes associated with the degradation of peptidoglycan (lysozymes). The protein level differences between C. elegans grown on native microbiome members compared to the laboratory food bacterium may help to identify molecular processes involved in host-microbe interactions.


Assuntos
Proteínas de Caenorhabditis elegans/metabolismo , Caenorhabditis elegans/microbiologia , Escherichia coli/fisiologia , Infecções por Bactérias Gram-Negativas/veterinária , Interações Hospedeiro-Patógeno , Microbiota , Ochrobactrum/fisiologia , Animais , Caenorhabditis elegans/metabolismo , Infecções por Bactérias Gram-Negativas/metabolismo , Proteômica , Transdução de Sinais , Espectrometria de Massas em Tandem
15.
BMC Biol ; 14: 38, 2016 05 09.
Artigo em Inglês | MEDLINE | ID: mdl-27160191

RESUMO

BACKGROUND: Host-microbe associations underlie many key processes of host development, immunity, and life history. Yet, none of the current research on the central model species Caenorhabditis elegans considers the worm's natural microbiome. Instead, almost all laboratories exclusively use the canonical strain N2 and derived mutants, maintained through routine bleach sterilization in monoxenic cultures with an E. coli strain as food. Here, we characterize for the first time the native microbiome of C. elegans and assess its influence on nematode life history characteristics. RESULTS: Nematodes sampled directly from their native habitats carry a species-rich bacterial community, dominated by Proteobacteria such as Enterobacteriaceae and members of the genera Pseudomonas, Stenotrophomonas, Ochrobactrum, and Sphingomonas. The C. elegans microbiome is distinct from that of the worm's natural environment and the congeneric species C. remanei. Exposure to a derived experimental microbiome revealed that bacterial composition is influenced by host developmental stage and genotype. These experiments also showed that the microbes enhance host fitness under standard and also stressful conditions (e.g., high temperature and either low or high osmolarity). Taking advantage of the nematode's transparency, we further demonstrate that several Proteobacteria are able to enter the C. elegans gut and that an Ochrobactrum isolate even seems to be able to persist in the intestines under stressful conditions. Moreover, three Pseudomonas isolates produce an anti-fungal effect in vitro which we show can contribute to the worm's defense against fungal pathogens in vivo. CONCLUSION: This first systematic analysis of the nematode's native microbiome reveals a species-rich bacterial community to be associated with C. elegans, which is likely of central importance for our understanding of the worm's biology. The information acquired and the microbial isolates now available for experimental work establishes C. elegans as a tractable model for the in-depth dissection of host-microbiome interactions.


Assuntos
Caenorhabditis elegans/microbiologia , Microbiota , Modelos Biológicos , Animais , Antifúngicos/metabolismo , Caenorhabditis elegans/crescimento & desenvolvimento , Estágios do Ciclo de Vida , Fenótipo , Proteobactérias/isolamento & purificação , Proteobactérias/metabolismo , Especificidade da Espécie
16.
Ecol Evol ; 5(16): 3250-63, 2015 Aug.
Artigo em Inglês | MEDLINE | ID: mdl-26380661

RESUMO

The nematode Caenorhabditis elegans is a central laboratory model system in almost all biological disciplines, yet its natural life history and population biology are largely unexplored. Such information is essential for in-depth understanding of the nematode's biology because its natural ecology provides the context, in which its traits and the underlying molecular mechanisms evolved. We characterized natural phenotypic and genetic variation among North German C. elegans isolates. We used the unique opportunity to compare samples collected 10 years apart from the same compost heap and additionally included recent samples for this and a second site, collected across a 1.5-year period. Our analysis revealed significant population genetic differentiation between locations, across the 10-year time period, but for only one location a trend across the shorter time frame. Significant variation was similarly found for phenotypic traits of likely importance in nature, such as choice behavior and population growth in the presence of pathogens or naturally associated bacteria. Phenotypic variation was significantly influenced by C. elegans genotype, time of isolation, and sampling site. The here studied C. elegans isolates may provide a valuable, genetically variable resource for future dissection of naturally relevant gene functions.

17.
BMC Ecol ; 15: 19, 2015 07 13.
Artigo em Inglês | MEDLINE | ID: mdl-26170141

RESUMO

BACKGROUND: How do very small animals with limited long-distance dispersal abilities move between locations, especially if they prefer ephemeral micro-habitats that are only available for short periods of time? The free-living model nematode Caenorhabditis elegans and several congeneric taxa appear to be common in such short-lived environments, for example decomposing fruits or other rotting plant material. Dispersal is usually assumed to depend on animal vectors, yet all current data is based on only a limited number of studies. In our project we performed three comprehensive field surveys on possible invertebrate vectors in North German locations containing populations of C. elegans and two related species, especially C. remanei, and combined these screens with an experimental analysis of persistence in one of the vector taxa. RESULTS: Our field survey revealed that Caenorhabditis nematodes are commonly found in slugs, isopods, and chilopods, but are not present in the remaining taxonomic groups examined. Surprisingly, the nematodes were frequently isolated from the intestines of slugs, even if slugs were not collected in close association with suitable substrates for Caenorhabditis proliferation. This suggests that the nematodes are able to enter the slug intestines and persist for certain periods of time. Our experimental analysis confirmed the ability of C. elegans to invade slug intestines and subsequently be excreted alive with the slug feces, although only for short time periods under laboratory conditions. CONCLUSIONS: We conclude that three invertebrate taxonomic groups represent potential vectors of Caenorhabditis nematodes. The nematodes appear to have evolved specific adaptations to enter and persist in the harsh environment of slug intestines, possibly indicating first steps towards a parasitic life-style.


Assuntos
Distribuição Animal , Caenorhabditis/fisiologia , Ecossistema , Gastrópodes/parasitologia , Animais , Caenorhabditis/classificação , Código de Barras de DNA Taxonômico , Gastrópodes/classificação , Alemanha , Intestinos/parasitologia , Isópodes , Dados de Sequência Molecular
18.
Trends Genet ; 31(3): 120-7, 2015 Mar.
Artigo em Inglês | MEDLINE | ID: mdl-25577479

RESUMO

Functional information about the large majority of the genes is still lacking in the classical eukaryotic model species Drosophila melanogaster, Caenorhabditis elegans, and Mus musculus. Because many of these genes are likely to be important in natural settings, considering explicit ecological information should increase our knowledge of gene function. Using C. elegans as an example, we discuss the importance of biotic factors as a driving force in shaping the composition and structure of the nematode genome. We highlight examples for which consideration of ecological information and natural variation have been key to the identification of novel, unexpected gene functions, and use these examples to define future research avenues for the classical genetic model taxa.


Assuntos
Caenorhabditis elegans/genética , Fenômenos Ecológicos e Ambientais , Genoma Helmíntico/genética , Animais , Evolução Biológica , Modelos Genéticos , Fenótipo
19.
BMC Ecol ; 14: 4, 2014 Feb 06.
Artigo em Inglês | MEDLINE | ID: mdl-24502455

RESUMO

BACKGROUND: Although the nematode Caenorhabditis elegans is a major model organism in diverse biological areas and well studied under laboratory conditions, little is known about its ecology. Therefore, characterization of the species' natural habitats should provide a new perspective on its otherwise well-studied biology. The currently best characterized populations are in France, demonstrating that C. elegans prefers nutrient- and microorganism-rich substrates such as rotting fruits and decomposing plant matter. In order to extend these findings, we sampled C. elegans continuously across 1.5 years from rotting apples and compost heaps in three North German locations. RESULTS: C. elegans was found throughout summer and autumn in both years. It shares its habitat with the related nematode species C. remanei, which could thus represent an important competitor for a similar ecological niche. The two species were isolated from the same site, but rarely the same substrate sample. In fact, C. elegans was mainly found on compost and C. remanei on rotten apples, possibly suggesting niche separation. The occurrence of C. elegans itself was related to environmental humidity and rain, although the correlation was significant for only one sampling site each. Additional associations between nematode prevalence and abiotic parameters could not be established. CONCLUSIONS: Taken together, our findings vary from the previous results for French C. elegans populations in that the considered German populations always coexisted with the congeneric species C. remanei (rather than C. briggsae as in France) and that C. elegans prevalence can associate with humidity and rain (rather than temperature, as suggested for French populations). Consideration of additional locations and time points is thus essential for full appreciation of the nematode's natural ecology.


Assuntos
Caenorhabditis elegans/isolamento & purificação , Ecossistema , Animais , Biodiversidade , Caenorhabditis/crescimento & desenvolvimento , Caenorhabditis/isolamento & purificação , Caenorhabditis elegans/crescimento & desenvolvimento , Frutas , Alemanha , Umidade , Malus , Dinâmica Populacional , Chuva , Estações do Ano , Solo
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