Microbial Species Coexistence Depends on the Host Environment

ABSTRACT Organisms and their resident microbial communities form a complex and mostly stable ecosystem. It is known that the specific composition and abundance of certain bacterial species affect host health and fitness, but the processes that lead to these microbial patterns are unknown. We investi...

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Autores principales: Peter Deines, Katrin Hammerschmidt, Thomas C. G. Bosch
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:122d5050127743f595c7569413c4441b2021-11-15T15:56:43ZMicrobial Species Coexistence Depends on the Host Environment10.1128/mBio.00807-202150-7511https://doaj.org/article/122d5050127743f595c7569413c4441b2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00807-20https://doaj.org/toc/2150-7511ABSTRACT Organisms and their resident microbial communities form a complex and mostly stable ecosystem. It is known that the specific composition and abundance of certain bacterial species affect host health and fitness, but the processes that lead to these microbial patterns are unknown. We investigate this by deconstructing the simple microbiome of the freshwater polyp Hydra. We contrast the performance of its two main bacterial associates, Curvibacter and Duganella, on germfree hosts with two in vitro environments over time. We show that interactions within the microbiome but also the host environment lead to the observed species frequencies and abundances. More specifically, we find that both microbial species can only stably coexist in the host environment, whereas Duganella outcompetes Curvibacter in both in vitro environments irrespective of initial starting frequencies. While Duganella seems to benefit through secretions of Curvibacter, its competitive effect on Curvibacter depends upon direct contact. The competition might potentially be mitigated through the spatial distribution of the two microbial species on the host, which would explain why both species stably coexist on the host. Interestingly, the relative abundances of both species on the host do not match the relative abundances reported previously nor the overall microbiome carrying capacity as reported in this study. Both observations indicate that rare microbial community members might be relevant for achieving the native community composition and carrying capacity. Our study highlights that for dissecting microbial interactions the specific environmental conditions need to be replicated, a goal difficult to achieve with in vitro systems. IMPORTANCE This work studies microbial interactions within the microbiome of the simple cnidarian Hydra and investigates whether microbial species coexistence and community stability depend on the host environment. We find that the outcome of the interaction between the two most dominant bacterial species in Hydra’s microbiome differs depending on the environment and results in a stable coexistence only in the host context. The interactive ecology between the host and the two most dominant microbes, but also the less abundant members of the microbiome, is critically important for achieving the native community composition. This indicates that the metaorganism environment needs to be taken into account when studying microbial interactions.Peter DeinesKatrin HammerschmidtThomas C. G. BoschAmerican Society for MicrobiologyarticleHydrahost-microbe interactionsmetaorganismmicrobiomespecies coexistenceMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution DOAJ
collection DOAJ
language EN
topic Hydra
host-microbe interactions
metaorganism
microbiome
species coexistence
Microbiology
QR1-502
spellingShingle Hydra
host-microbe interactions
metaorganism
microbiome
species coexistence
Microbiology
QR1-502
Peter Deines
Katrin Hammerschmidt
Thomas C. G. Bosch
Microbial Species Coexistence Depends on the Host Environment
description ABSTRACT Organisms and their resident microbial communities form a complex and mostly stable ecosystem. It is known that the specific composition and abundance of certain bacterial species affect host health and fitness, but the processes that lead to these microbial patterns are unknown. We investigate this by deconstructing the simple microbiome of the freshwater polyp Hydra. We contrast the performance of its two main bacterial associates, Curvibacter and Duganella, on germfree hosts with two in vitro environments over time. We show that interactions within the microbiome but also the host environment lead to the observed species frequencies and abundances. More specifically, we find that both microbial species can only stably coexist in the host environment, whereas Duganella outcompetes Curvibacter in both in vitro environments irrespective of initial starting frequencies. While Duganella seems to benefit through secretions of Curvibacter, its competitive effect on Curvibacter depends upon direct contact. The competition might potentially be mitigated through the spatial distribution of the two microbial species on the host, which would explain why both species stably coexist on the host. Interestingly, the relative abundances of both species on the host do not match the relative abundances reported previously nor the overall microbiome carrying capacity as reported in this study. Both observations indicate that rare microbial community members might be relevant for achieving the native community composition and carrying capacity. Our study highlights that for dissecting microbial interactions the specific environmental conditions need to be replicated, a goal difficult to achieve with in vitro systems. IMPORTANCE This work studies microbial interactions within the microbiome of the simple cnidarian Hydra and investigates whether microbial species coexistence and community stability depend on the host environment. We find that the outcome of the interaction between the two most dominant bacterial species in Hydra’s microbiome differs depending on the environment and results in a stable coexistence only in the host context. The interactive ecology between the host and the two most dominant microbes, but also the less abundant members of the microbiome, is critically important for achieving the native community composition. This indicates that the metaorganism environment needs to be taken into account when studying microbial interactions.
format article
author Peter Deines
Katrin Hammerschmidt
Thomas C. G. Bosch
author_facet Peter Deines
Katrin Hammerschmidt
Thomas C. G. Bosch
author_sort Peter Deines
title Microbial Species Coexistence Depends on the Host Environment
title_short Microbial Species Coexistence Depends on the Host Environment
title_full Microbial Species Coexistence Depends on the Host Environment
title_fullStr Microbial Species Coexistence Depends on the Host Environment
title_full_unstemmed Microbial Species Coexistence Depends on the Host Environment
title_sort microbial species coexistence depends on the host environment
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/122d5050127743f595c7569413c4441b
work_keys_str_mv AT peterdeines microbialspeciescoexistencedependsonthehostenvironment
AT katrinhammerschmidt microbialspeciescoexistencedependsonthehostenvironment
AT thomascgbosch microbialspeciescoexistencedependsonthehostenvironment
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