Wetlands harbor lactic acid-driven chain elongators

ABSTRACT Wetlands are globally significant carbon storage hotspots. Recent research has suggested that microbially derived metabolites may contribute to soil organic matter formation. Identifying pathways driving the formation of such metabolites is critical to understand the global impact of wetlan...

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Main Authors: Pieter Candry, Zachary Flinkstrom, Mari-Karoliina Henriikka Winkler
Format: Article
Language:English
Published: American Society for Microbiology 2024-01-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02105-23
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author Pieter Candry
Zachary Flinkstrom
Mari-Karoliina Henriikka Winkler
author_facet Pieter Candry
Zachary Flinkstrom
Mari-Karoliina Henriikka Winkler
author_sort Pieter Candry
collection DOAJ
description ABSTRACT Wetlands are globally significant carbon storage hotspots. Recent research has suggested that microbially derived metabolites may contribute to soil organic matter formation. Identifying pathways driving the formation of such metabolites is critical to understand the global impact of wetland carbon cycling. Here, we evaluate the presence of chain-elongating organisms converting two to three carbon compounds (i.e., lactic and acetic acid) to medium-chain carboxylic acids (MCCA; i.e., six-carbon caproic acid) in wetland soils. We demonstrate the enrichment of a lactic acid-driven chain-elongating community from wetland soils producing a mixture of butyric and caproic acid. The enriched community was dominated by Clostridiaceae, Ruminococcaceae, and Lachnospiraceae, three families with known chain elongators. Amplicon sequencing identified three Ruminococcaceae and one Clostridiaceae zero-radius OTU (zOTU) that were (i) present in the soil, (ii) enriched over 1% relative abundance in the bioreactor, and (iii) were closely related to known chain elongators. Moreover, close relatives of the three Ruminococcaceae zOTU were also observed in several other wetland microbiomes. From this observation, we conclude that close relatives of known chain elongators, potentially capable of lactic acid-driven MCCA production themselves, are present in wetland soils. This observation may have implications for our understanding of carbon cycling and storage in wetland ecosystems. IMPORTANCE Wetlands are globally significant carbon cycling hotspots that both sequester large amounts of CO2 as soil carbon as well as emit a third of all CH4 globally. Their outsized role in the global carbon cycle makes it critical to understand microbial processes contributing to carbon breakdown and storage in these ecosystems. Here, we confirm the presence of chain-elongating organisms in freshwater wetland soils. These organisms take small carbon compounds formed during the breakdown of biomass and turn them into larger compounds (six to eight carbon organic acids) that may potentially contribute to the formation of soil organic matter and long-term carbon storage. Moreover, we find that these chain-elongating organisms may be widely distributed in wetlands globally. Future work should identify these organisms’ contribution to carbon cycling in wetlands and the potential role of the products they form in carbon sequestration in wetlands.
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spelling doaj.art-28e161ebf0e945ce8401caee1421cb912024-01-11T14:04:37ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-01-0112110.1128/spectrum.02105-23Wetlands harbor lactic acid-driven chain elongatorsPieter Candry0Zachary Flinkstrom1Mari-Karoliina Henriikka Winkler2Civil and Environmental Engineering, University of Washington , Seattle, Washington, USACivil and Environmental Engineering, University of Washington , Seattle, Washington, USACivil and Environmental Engineering, University of Washington , Seattle, Washington, USAABSTRACT Wetlands are globally significant carbon storage hotspots. Recent research has suggested that microbially derived metabolites may contribute to soil organic matter formation. Identifying pathways driving the formation of such metabolites is critical to understand the global impact of wetland carbon cycling. Here, we evaluate the presence of chain-elongating organisms converting two to three carbon compounds (i.e., lactic and acetic acid) to medium-chain carboxylic acids (MCCA; i.e., six-carbon caproic acid) in wetland soils. We demonstrate the enrichment of a lactic acid-driven chain-elongating community from wetland soils producing a mixture of butyric and caproic acid. The enriched community was dominated by Clostridiaceae, Ruminococcaceae, and Lachnospiraceae, three families with known chain elongators. Amplicon sequencing identified three Ruminococcaceae and one Clostridiaceae zero-radius OTU (zOTU) that were (i) present in the soil, (ii) enriched over 1% relative abundance in the bioreactor, and (iii) were closely related to known chain elongators. Moreover, close relatives of the three Ruminococcaceae zOTU were also observed in several other wetland microbiomes. From this observation, we conclude that close relatives of known chain elongators, potentially capable of lactic acid-driven MCCA production themselves, are present in wetland soils. This observation may have implications for our understanding of carbon cycling and storage in wetland ecosystems. IMPORTANCE Wetlands are globally significant carbon cycling hotspots that both sequester large amounts of CO2 as soil carbon as well as emit a third of all CH4 globally. Their outsized role in the global carbon cycle makes it critical to understand microbial processes contributing to carbon breakdown and storage in these ecosystems. Here, we confirm the presence of chain-elongating organisms in freshwater wetland soils. These organisms take small carbon compounds formed during the breakdown of biomass and turn them into larger compounds (six to eight carbon organic acids) that may potentially contribute to the formation of soil organic matter and long-term carbon storage. Moreover, we find that these chain-elongating organisms may be widely distributed in wetlands globally. Future work should identify these organisms’ contribution to carbon cycling in wetlands and the potential role of the products they form in carbon sequestration in wetlands.https://journals.asm.org/doi/10.1128/spectrum.02105-23wetlandcarbon cyclechain elongationmedium-chain carboxylic acids
spellingShingle Pieter Candry
Zachary Flinkstrom
Mari-Karoliina Henriikka Winkler
Wetlands harbor lactic acid-driven chain elongators
Microbiology Spectrum
wetland
carbon cycle
chain elongation
medium-chain carboxylic acids
title Wetlands harbor lactic acid-driven chain elongators
title_full Wetlands harbor lactic acid-driven chain elongators
title_fullStr Wetlands harbor lactic acid-driven chain elongators
title_full_unstemmed Wetlands harbor lactic acid-driven chain elongators
title_short Wetlands harbor lactic acid-driven chain elongators
title_sort wetlands harbor lactic acid driven chain elongators
topic wetland
carbon cycle
chain elongation
medium-chain carboxylic acids
url https://journals.asm.org/doi/10.1128/spectrum.02105-23
work_keys_str_mv AT pietercandry wetlandsharborlacticaciddrivenchainelongators
AT zacharyflinkstrom wetlandsharborlacticaciddrivenchainelongators
AT marikaroliinahenriikkawinkler wetlandsharborlacticaciddrivenchainelongators