Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.

BACKGROUND: Earthworms play a critical role in organic matter decomposition because of the interactions they establish with microorganisms. The ingestion, digestion, assimilation of organic material in the gut and then casting is the first step in earthworm-microorganism interactions. The current kn...

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Main Authors: María Gómez-Brandón, Manuel Aira, Marta Lores, Jorge Domínguez
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3174214?pdf=render
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spelling doaj-de6b44e397954a099aadb819669eba342020-11-25T01:25:03ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0169e2478610.1371/journal.pone.0024786Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.María Gómez-BrandónManuel AiraMarta LoresJorge DomínguezBACKGROUND: Earthworms play a critical role in organic matter decomposition because of the interactions they establish with microorganisms. The ingestion, digestion, assimilation of organic material in the gut and then casting is the first step in earthworm-microorganism interactions. The current knowledge of these direct effects is still limited for epigeic earthworm species, mainly those living in man-made environments. Here we tested whether and to what extent the earthworm Eisenia andrei is capable of altering the microbiological properties of fresh organic matter through gut associated processes; and if these direct effects are related to the earthworm diet. METHODOLOGY: To address these questions we determined the microbial community structure (phospholipid fatty acid profiles) and microbial activity (fluorescein diacetate hydrolysis) in the earthworm casts derived from three types of animal manure (cow, horse and pig manure), which differed in microbial composition. PRINCIPAL FINDINGS: The passage of the organic material through the gut of E. andrei reduced the total microbial biomass irrespective of the type of manure, and resulted in a decrease in bacterial biomass in all the manures; whilst leaving the fungi unaffected in the egested materials. However, unlike the microbial biomass, no such reduction was detected in the total microbial activity of cast samples derived from the pig manure. Moreover, no differences were found between cast samples derived from the different types of manure with regards to microbial community structure, which provides strong evidence for a bottleneck effect of worm digestion on microbial populations of the original material consumed. CONCLUSIONS/SIGNIFICANCE: Our data reveal that earthworm gut is a major shaper of microbial communities, thereby favouring the existence of a reduced but more active microbial population in the egested materials, which is of great importance to understand how biotic interactions within the decomposer food web influence on nutrient cycling.http://europepmc.org/articles/PMC3174214?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author María Gómez-Brandón
Manuel Aira
Marta Lores
Jorge Domínguez
spellingShingle María Gómez-Brandón
Manuel Aira
Marta Lores
Jorge Domínguez
Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
PLoS ONE
author_facet María Gómez-Brandón
Manuel Aira
Marta Lores
Jorge Domínguez
author_sort María Gómez-Brandón
title Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
title_short Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
title_full Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
title_fullStr Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
title_full_unstemmed Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
title_sort epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2011-01-01
description BACKGROUND: Earthworms play a critical role in organic matter decomposition because of the interactions they establish with microorganisms. The ingestion, digestion, assimilation of organic material in the gut and then casting is the first step in earthworm-microorganism interactions. The current knowledge of these direct effects is still limited for epigeic earthworm species, mainly those living in man-made environments. Here we tested whether and to what extent the earthworm Eisenia andrei is capable of altering the microbiological properties of fresh organic matter through gut associated processes; and if these direct effects are related to the earthworm diet. METHODOLOGY: To address these questions we determined the microbial community structure (phospholipid fatty acid profiles) and microbial activity (fluorescein diacetate hydrolysis) in the earthworm casts derived from three types of animal manure (cow, horse and pig manure), which differed in microbial composition. PRINCIPAL FINDINGS: The passage of the organic material through the gut of E. andrei reduced the total microbial biomass irrespective of the type of manure, and resulted in a decrease in bacterial biomass in all the manures; whilst leaving the fungi unaffected in the egested materials. However, unlike the microbial biomass, no such reduction was detected in the total microbial activity of cast samples derived from the pig manure. Moreover, no differences were found between cast samples derived from the different types of manure with regards to microbial community structure, which provides strong evidence for a bottleneck effect of worm digestion on microbial populations of the original material consumed. CONCLUSIONS/SIGNIFICANCE: Our data reveal that earthworm gut is a major shaper of microbial communities, thereby favouring the existence of a reduced but more active microbial population in the egested materials, which is of great importance to understand how biotic interactions within the decomposer food web influence on nutrient cycling.
url http://europepmc.org/articles/PMC3174214?pdf=render
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