Insights into the earthworm gut multi-kingdom microbial communities

Rumakanta Sapkota; Susana Santos; Pedro Daniel Geadas Farias; Paul Henning Krogh; Anne Winding

doi:10.1016/j.scitotenv.2020.138301

Insights into the earthworm gut multi-kingdom microbial communities

Rumakanta Sapkota, Susana Santos, Pedro Daniel Geadas Farias, Paul Henning Krogh, Anne Winding

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

72 Citations (Scopus)

Abstract

Earthworms are widely known to impact soil health, having a key
role in nutrient cycling and are often referred to as soil engineers.
They are vital for soil microbial assemblages particularly through their
feeding and burrowing activity in soil. Earthworms feed on soil organic
matter and litter, and the resulting casts alter the soil microbial
community. However, the gut microbiome of earthworms remains less known.
In this study, we used amplicon sequencing of the 16S rRNA gene for
bacteria and 18S rRNA gene for eukaryotes to assess the gut community
assemblages of earthworm species within three genera Aporrectodea,
Allolobophora and Lumbricus that represent different life forms sharing
the same habitat. The objective was to compare the gut microbiome
profiles of eukaryotic and prokaryotic organisms to assess significance
of earthworm life forms, and to explore the cross kingdom networks in an
attempt to identify keystone species. We found a high eukaryotic
diversity with a dominance of the SAR supergroup along with fungi and
metazoan in the earthworm gut. The bacterial community were dominated by
members of Proteobacteria, Acidobacteria, Actinobacteria, Firmicutes, and
Verrucomicrobia. The eukaryotic and prokaryotic communities showed
similar differences in alpha diversity, being lowest in Lumbricus
herculeus. The beta diversity showed earthworm species as a key factor in
shaping gut microbiomes with L. herculeus harboring distinct microbiomes
compared to species of Aporrectodea caliginosa, A. longa, A. tuberculata
and Allolobophora chlorotica. Cross kingdom networks showed high
interactions between several protist and bacterial OTUs. In conclusion,
this study suggested that the community assemblages of gut microbiomes
was shaped by earthworm species and life form, and such assemblage
consist of cross kingdom interactions among eukaryotes and prokaryotes.

Original language	English
Article number	138301
Journal	Science of the Total Environment
Volume	727
ISSN	0048-9697
DOIs	https://doi.org/10.1016/j.scitotenv.2020.138301
Publication status	Published - Jul 2020

Keywords

Microbiomes
Protists
Eukaryotic microbes
eDNA
metabarcoding
amplicon sequencing

Access to Document

10.1016/j.scitotenv.2020.138301

1 Active
3 Finished

Center for DNA baserede metoder og kompetencer til biomonitering
Winding, A. (Project coordinator), Hansen, L. H. (Project manager), Krogh, P. H. (Project manager), Stæhr, P. A. (Participant), Andersen, L. W. (Participant), Wiberg-Larsen, P. (Participant), Santos, S. (Participant), Browne, P. D. (Participant) & Sapkota, R. (Participant)
01/07/2015 → …
Project: Research
eDNA Center - Applied molecular tools for environmental monitoring and research
Winding, A. (PI), Sapkota, R. (PI), Zervas, T. (PI), Hendriksen, N. B. (PI), Stougaard, P. (PI), Thøgersen, M. S. (PI), Barbosa Anesio, A. M. (PI), Zeng, Y. (PI), Johansen, A. (PI), Jacobsen, C. S. (PI), Ørby, P. V. (PI), Stæhr, P. A. (PI), Hansen, J. L. S. (PI), Jakobsen, H. (PI), Krause-Jensen, D. (PI), Krogh, P. H. (PI), Schmidt, N. M. (PI), Scheel, M. (PI), Andersen, L. W. (PI), Nicolaisen, M. (PI), Madsen, M. V. (PI), Santos, S. (PI), Kudjordjie, E. N. (PI) & Sikder, M. M. (PI)
01/01/2020 → 30/11/2023
Project: Research
Natedna: eDNA i Naturovervågningen
Winding, A. (Project manager), Andersen, L. W. (Participant), Hansen, M. M. (Participant), Krause-Jensen, D. (Participant), Krogh, P. H. (Participant), Hansen, L. H. (Participant), Hendriksen, N. B. (Participant), Nicolaisen, M. (Participant), Panitz, F. (Participant) & Stæhr, P. A. (Participant)
01/06/2017 → 31/12/2018
Project: Research

COST ACTION Soil fauna - Key to Soil Organic Matter Dynamics and Modelling (KEYSOM)
Krogh, P. H. (Member)
15 Jul 2015 → 15 Mar 2019
Activity: Presentations, memberships, employment, ownership and other activities › Member of research network

Cite this

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title = "Insights into the earthworm gut multi-kingdom microbial communities",

abstract = "Earthworms are widely known to impact soil health, having a keyrole in nutrient cycling and are often referred to as soil engineers.They are vital for soil microbial assemblages particularly through theirfeeding and burrowing activity in soil. Earthworms feed on soil organicmatter and litter, and the resulting casts alter the soil microbialcommunity. However, the gut microbiome of earthworms remains less known.In this study, we used amplicon sequencing of the 16S rRNA gene forbacteria and 18S rRNA gene for eukaryotes to assess the gut communityassemblages of earthworm species within three genera Aporrectodea,Allolobophora and Lumbricus that represent different life forms sharingthe same habitat. The objective was to compare the gut microbiomeprofiles of eukaryotic and prokaryotic organisms to assess significanceof earthworm life forms, and to explore the cross kingdom networks in anattempt to identify keystone species. We found a high eukaryoticdiversity with a dominance of the SAR supergroup along with fungi andmetazoan in the earthworm gut. The bacterial community were dominated bymembers of Proteobacteria, Acidobacteria, Actinobacteria, Firmicutes, andVerrucomicrobia. The eukaryotic and prokaryotic communities showedsimilar differences in alpha diversity, being lowest in Lumbricusherculeus. The beta diversity showed earthworm species as a key factor inshaping gut microbiomes with L. herculeus harboring distinct microbiomescompared to species of Aporrectodea caliginosa, A. longa, A. tuberculataand Allolobophora chlorotica. Cross kingdom networks showed highinteractions between several protist and bacterial OTUs. In conclusion,this study suggested that the community assemblages of gut microbiomeswas shaped by earthworm species and life form, and such assemblageconsist of cross kingdom interactions among eukaryotes and prokaryotes.",

keywords = "Microbiomes, Protists, Eukaryotic microbes, eDNA, metabarcoding, amplicon sequencing",

author = "Rumakanta Sapkota and Susana Santos and Farias, {Pedro Daniel Geadas} and Krogh, {Paul Henning} and Anne Winding",

year = "2020",

month = jul,

doi = "10.1016/j.scitotenv.2020.138301",

language = "English",

volume = "727",

journal = "Science of the Total Environment",

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T1 - Insights into the earthworm gut multi-kingdom microbial communities

AU - Sapkota, Rumakanta

AU - Santos, Susana

AU - Farias, Pedro Daniel Geadas

AU - Krogh, Paul Henning

AU - Winding, Anne

PY - 2020/7

Y1 - 2020/7

N2 - Earthworms are widely known to impact soil health, having a keyrole in nutrient cycling and are often referred to as soil engineers.They are vital for soil microbial assemblages particularly through theirfeeding and burrowing activity in soil. Earthworms feed on soil organicmatter and litter, and the resulting casts alter the soil microbialcommunity. However, the gut microbiome of earthworms remains less known.In this study, we used amplicon sequencing of the 16S rRNA gene forbacteria and 18S rRNA gene for eukaryotes to assess the gut communityassemblages of earthworm species within three genera Aporrectodea,Allolobophora and Lumbricus that represent different life forms sharingthe same habitat. The objective was to compare the gut microbiomeprofiles of eukaryotic and prokaryotic organisms to assess significanceof earthworm life forms, and to explore the cross kingdom networks in anattempt to identify keystone species. We found a high eukaryoticdiversity with a dominance of the SAR supergroup along with fungi andmetazoan in the earthworm gut. The bacterial community were dominated bymembers of Proteobacteria, Acidobacteria, Actinobacteria, Firmicutes, andVerrucomicrobia. The eukaryotic and prokaryotic communities showedsimilar differences in alpha diversity, being lowest in Lumbricusherculeus. The beta diversity showed earthworm species as a key factor inshaping gut microbiomes with L. herculeus harboring distinct microbiomescompared to species of Aporrectodea caliginosa, A. longa, A. tuberculataand Allolobophora chlorotica. Cross kingdom networks showed highinteractions between several protist and bacterial OTUs. In conclusion,this study suggested that the community assemblages of gut microbiomeswas shaped by earthworm species and life form, and such assemblageconsist of cross kingdom interactions among eukaryotes and prokaryotes.

AB - Earthworms are widely known to impact soil health, having a keyrole in nutrient cycling and are often referred to as soil engineers.They are vital for soil microbial assemblages particularly through theirfeeding and burrowing activity in soil. Earthworms feed on soil organicmatter and litter, and the resulting casts alter the soil microbialcommunity. However, the gut microbiome of earthworms remains less known.In this study, we used amplicon sequencing of the 16S rRNA gene forbacteria and 18S rRNA gene for eukaryotes to assess the gut communityassemblages of earthworm species within three genera Aporrectodea,Allolobophora and Lumbricus that represent different life forms sharingthe same habitat. The objective was to compare the gut microbiomeprofiles of eukaryotic and prokaryotic organisms to assess significanceof earthworm life forms, and to explore the cross kingdom networks in anattempt to identify keystone species. We found a high eukaryoticdiversity with a dominance of the SAR supergroup along with fungi andmetazoan in the earthworm gut. The bacterial community were dominated bymembers of Proteobacteria, Acidobacteria, Actinobacteria, Firmicutes, andVerrucomicrobia. The eukaryotic and prokaryotic communities showedsimilar differences in alpha diversity, being lowest in Lumbricusherculeus. The beta diversity showed earthworm species as a key factor inshaping gut microbiomes with L. herculeus harboring distinct microbiomescompared to species of Aporrectodea caliginosa, A. longa, A. tuberculataand Allolobophora chlorotica. Cross kingdom networks showed highinteractions between several protist and bacterial OTUs. In conclusion,this study suggested that the community assemblages of gut microbiomeswas shaped by earthworm species and life form, and such assemblageconsist of cross kingdom interactions among eukaryotes and prokaryotes.

KW - Microbiomes

KW - Protists

KW - Eukaryotic microbes

KW - eDNA

KW - metabarcoding

KW - amplicon sequencing

U2 - 10.1016/j.scitotenv.2020.138301

DO - 10.1016/j.scitotenv.2020.138301

M3 - Journal article

C2 - 32330704

SN - 0048-9697

VL - 727

JO - Science of the Total Environment

JF - Science of the Total Environment

M1 - 138301

ER -

Insights into the earthworm gut multi-kingdom microbial communities

Abstract

Keywords

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Projects

Center for DNA baserede metoder og kompetencer til biomonitering

eDNA Center - Applied molecular tools for environmental monitoring and research

Natedna: eDNA i Naturovervågningen

Activities

COST ACTION Soil fauna - Key to Soil Organic Matter Dynamics and Modelling (KEYSOM)

Cite this