Dataset Information

Differential Engagement of Fermentative Taxa in Gut Contents of the Earthworm Lumbricus terrestris.

ABSTRACT: The earthworm gut is an anoxic, saccharide-rich microzone in aerated soils. The apparent degradation of diverse saccharides in the alimentary canal of the model earthworm Lumbricusterrestris is concomitant with the production of diverse organic acids, indicating that fermentation is an ongoing process in the earthworm gut. However, little is known about how different gut-associated saccharides are fermented. The hypothesis of this investigation was that different gut-associated saccharides differentially stimulate fermentative microorganisms in gut contents of L. terrestris This hypothesis was addressed by (i) assessing the fermentation profiles of anoxic gut content microcosms that were supplemented with gut-associated saccharides and (ii) the concomitant phylogenic analysis of 16S rRNA sequences. Galactose, glucose, maltose, mannose, arabinose, fucose, rhamnose, and xylose stimulated the production of fermentation products, including H2, CO2, acetate, lactate, propionate, formate, succinate, and ethanol. Fermentation profiles were dependent on the supplemental saccharide (e.g., glucose yielded large amounts of H2 and ethanol, whereas fucose did not, and maltose yielded large amounts of lactate, whereas mannose did not). Approximately 1,750,000 16S rRNA sequences were affiliated with 37 families, and phylogenic analyses indicated that a respective saccharide stimulated a subset of the diverse phylotypes. An Aeromonas-related phylotype displayed a high relative abundance in all treatments, whereas key Enterobacteriaceae-affiliated phylotypes were stimulated by some but not all saccharides. Collectively, these results reinforce the likelihood that (i) different saccharides stimulate different fermentations in gut contents of the earthworm and (ii) facultative aerobes related to Aeromonadaceae and Enterobacteriaceae can be important drivers of these fermentations.IMPORTANCE The feeding habits of earthworms influence the turnover of elements in the terrestrial biosphere. The alimentary tract of the earthworm constitutes an anoxic saccharide-rich microzone in aerated soils that offers ingested microbes a unique opportunity for anaerobic growth. The fermentative activity of microbes in the alimentary tract are responsible for the in situ production of (i) organic compounds that can be assimilated by the earthworm and (ii) H2 that is subject to in vivo emission by the earthworm and can be trophically linked to secondary microbial events in soils. To gain insight on how fermentative members of the gut microbiome might respond to the saccharide-rich alimentary canal, this study examines the impact of diverse gut-associated saccharides on the differential activation of fermentative microbes in gut contents of the model earthworm L. terrestris.

SUBMITTER: Meier AB

PROVIDER: S-EPMC5812936 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Differential Engagement of Fermentative Taxa in Gut Contents of the Earthworm Lumbricus terrestris.

Meier Anja B AB Hunger Sindy S Drake Harold L HL

Applied and environmental microbiology 20180214 5

The earthworm gut is an anoxic, saccharide-rich microzone in aerated soils. The apparent degradation of diverse saccharides in the alimentary canal of the model earthworm <i>Lumbricus</i><i>terrestris</i> is concomitant with the production of diverse organic acids, indicating that fermentation is an ongoing process in the earthworm gut. However, little is known about how different gut-associated saccharides are fermented. The hypothesis of this investigation was that different gut-associated sac ...[more]

PMID: 29247057

Similar Datasets

Project description:Earthworms are a dominant macrofauna in soil ecosystems and have determinative effects on soil fertility and plant growth. These invertebrates feed on ingested material, and gizzard-linked disruption of ingested fungal and bacterial cells is conceived to provide diverse biopolymers in the anoxic alimentary canals of earthworms. Fermentation in the gut is likely important to the utilization of ingested biopolymer-derived compounds by the earthworm. This study therefore examined the fermentative responses of gut content-associated microbes of the model earthworm Lumbricus terrestris to (i) microbial cell lysate (to simulate gizzard-disrupted cells) and (ii) dominant biopolymers of such biomass, protein, and RNA. The microbial cell lysate augmented the production of H2, CO2, and diverse fatty acids (e.g., formate, acetate, propionate, succinate, and butyrate) in anoxic gut content microcosms, indicating that the cell lysate triggered diverse fermentations. Protein and RNA also augmented diverse fermentations in anoxic microcosms of gut contents, each yielding a distinct product profile (e.g., RNA yielded H2 and succinate, whereas protein did not). The combined product profile of protein and RNA treatments was similar to that of cell lysate treatments, and 16S rRNA-based analyses indicated that many taxa that responded to cell lysate were similar to taxa that responded to protein or RNA. In particular, protein stimulated Peptostreptococcaceae, Clostridiaceae, and Fusobacteriaceae, whereas RNA stimulated Aeromonadaceae These findings demonstrate the capacity of gut-associated obligate anaerobes and facultative aerobes to catalyze biopolymer-driven fermentations and highlight the potential importance of protein and RNA as substrates linked to the overall turnover dynamics of organic carbon in the alimentary canal of the earthworm.IMPORTANCE The subsurface lifestyle of earthworms makes them an unnoticed component of the terrestrial biosphere. However, the propensity of these invertebrates to consume their home, i.e., soil and litter, has long-term impacts on soil fertility, plant growth, and the cycling of elements. The alimentary canals of earthworms can contain up to 500 ml anoxic gut content per square meter of soil, and ingested soil may contain 109 or more microbial cells per gram dry weight, considerations that illustrate that enormous numbers of soil microbes are subject to anoxia during gut passage. Feeding introduces diverse sources of biopolymers to the gut, and the gut fermentation of biopolymers could be important to the transformation of matter by the earthworm and its capacity to utilize fermentation-derived fatty acids. Thus, this study examined the capacity of microbes in earthworm gut contents to ferment protein and RNA, dominant biopolymers of cells that become disrupted during gut passage.

Project description:Biochar is the degradation-resistant product generated by the pyrolysis of organic materials and is produced for the intended use of land application in order to promote carbon sequestration and soil improvement. However, despite the many potential benefits biochar application offers, it is important to quantify any ecological impacts that may result from soil amendment in order to avoid potentially causing negative effects upon soil biota which are crucial in the many ecosystem services provided by soil. Any impacts on earthworms in particular are important to evaluate because of their pivotal role in organic matter breakdown, nutrient cycling and soil formation. In this study, we conducted a series of ecotoxicological assays to determine lethal and sublethal (avoidance, mass change and moisture content) effects of heavy biochar applications that reflect levels that may be used in soil restoration efforts. Two earthworm species, Eisenia fetida, an epigeic species, and Lumbricus terrestris, an anecic species, were utilised as test organisms. Two types of biochar, produced from wheat straw and rice husk feedstocks, respectively, were applied to OECD artificial soil and to a natural soil (Kettering loam) at rates of up to 20% w/w. The influence of biochar application on soil porewater chloride, fluoride and phosphate concentrations was also assessed. The biochar applications induced only a subtle level of avoidance behaviour while effects on survival over a 4-week exposure period were inconsistent. However, death and physical damage to some individual earthworms at high biochar application rates were observed, the mechanisms and processes leading to which should be investigated further. Earthworm development (mean mass change over time) proved to be a more sensitive measure, revealing negative effects on L. terrestris at 10% and 20% (w/w) wheat biochar applications in OECD soil and at 20% (w/w) applications of both biochars in Kettering loam. The moisture content of E. fetida remained remarkably consistent across all treatments (~ 82%), indicating that this is not a sensitive measure of effects. The high rates of biochar application resulted in increased chloride (2 to 3-fold) and phosphate (100-fold) concentrations in simulated soil porewaters, which has important implications for soil fertility and production but also for environmental management.

Dataset Information

Differential Engagement of Fermentative Taxa in Gut Contents of the Earthworm Lumbricus terrestris.

Publications

Differential Engagement of Fermentative Taxa in Gut Contents of the Earthworm Lumbricus terrestris.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets