Dynamics of carbon substrate competition among heterotrophic microorganisms

Author(s)McNichol, Samuel M.
Author(s)Sanchez-Quete, Fernando
Author(s)Loeb, Stephanie K.
Author(s)Teske, Andreas P.
Author(s)Walter, Sunita R Shah
Author(s)Mahmoudi, Nagissa
Date Accessioned2024-04-05T18:53:32Z
Date Available2024-04-05T18:53:32Z
Publication Date2024-01-29
DescriptionThis article was originally published in The ISME Journal: Multidisciplinary Journal of Microbial Ecology. The version of record is available at: https://doi.org/10.1093/ismejo/wrae018. © The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
AbstractGrowing evidence suggests that interactions among heterotrophic microorganisms influence the efficiency and rate of organic matter turnover. These interactions are dynamic and shaped by the composition and availability of resources in their surrounding environment. Heterotrophic microorganisms inhabiting marine environments often encounter fluctuations in the quality and quantity of carbon inputs, ranging from simple sugars to large, complex compounds. Here, we experimentally tested how the chemical complexity of carbon substrates affects competition and growth dynamics between two heterotrophic marine isolates. We tracked cell density using species-specific polymerase chain reaction (PCR) assays and measured rates of microbial CO2 production along with associated isotopic signatures (13C and 14C) to quantify the impact of these interactions on organic matter remineralization. The observed cell densities revealed substrate-driven interactions: one species exhibited a competitive advantage and quickly outgrew the other when incubated with a labile compound whereas both species seemed to coexist harmoniously in the presence of more complex organic matter. Rates of CO2 respiration revealed that coincubation of these isolates enhanced organic matter turnover, sometimes by nearly 2-fold, compared to their incubation as mono-cultures. Isotopic signatures of respired CO2 indicated that coincubation resulted in a greater remineralization of macromolecular organic matter. These results demonstrate that simple substrates promote competition whereas high substrate complexity reduces competitiveness and promotes the partitioning of degradative activities into distinct niches, facilitating coordinated utilization of the carbon pool. Taken together, this study yields new insight into how the quality of organic matter plays a pivotal role in determining microbial interactions within marine environments.
SponsorThis work was supported by grants from the U.S. National Science Foundation award (no. 2023656) and Fonds de recherche du Quebec—Nature et technologies (FRQNT) grant (no. 283357). Targeted on- and off-axis sampling in Guaymas Basin was made possible by U.S. National Science Foundation grant (no. 1357238) to A.T., and the excellent performance of the “Alvin” and “Sentry” teams during cruise AT37-06).
CitationSamuel M McNichol, Fernando Sanchez-Quete, Stephanie K Loeb, Andreas P Teske, Sunita R Shah Walter, Nagissa Mahmoudi, Dynamics of carbon substrate competition among heterotrophic microorganisms, The ISME Journal, Volume 18, Issue 1, January 2024, wrae018, https://doi.org/10.1093/ismejo/wrae018
ISSN1751-7370
URLhttps://udspace.udel.edu/handle/19716/34248
Languageen_US
PublisherThe ISME Journal: Multidisciplinary Journal of Microbial Ecology
dc.rightsAttribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
Keywordsmicrobial interactions
Keywordscompetition
Keywordsmarine bacteria
Keywordscarbon cycling
Keywordsorganic matter
Keywordsclimate action
Keywordslife on land
TitleDynamics of carbon substrate competition among heterotrophic microorganisms
TypeArticle
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