Interspecies interactions mediated by conductive minerals in the sediments of the iron rich meromictic Lake La Cruz, Spain

Amelia-Elena Rotaru*, Nicole Posth, Carolin Löscher, Maria R. Miracle, Eduardo Vincence, Raymond Pickett Cox, Jennifer Thompson, Simon W. Poulton, Bo Thamdrup

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. Here we show that conductive particles drove the metabolic coupling between electroactive microbial clades from this environment. The anoxic sediment of Lake La Cruz was rich in biogeochemically ‘reactive’ iron minerals, and harbored known electroactive species such as Geobacter and Methanothrix, in addition to groups not ever linked to an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed 2 to 4 times higher methanogenic activity, as compared to incubations with non-conductive glass beads or without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated above 8 mM depending on substrate (8 ± 0.6 to 11.7 ± 1.2 mM). Only by enabling syntrophic acetate oxidation with conductive minerals we could prevent acetate accumulation. Acetate oxidation conductively coupled to methanogenic activity had a stoichiometric recovery of 70% and could be maintained in subsequent transfers if and only if amended with conductive particles. Mud-free enrichments without conductive particles ceased any metabolic activity after the second transfer. Conductive particles preserved a consortium of Youngiibacter-Methanothrix, whereas without conductive particles Youngiibacter spp. died off. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles inferring that minerals may have arbitrated the earliest interspecies associations
Original languageEnglish
JournalLimnetica
Volume38
Issue number1
Pages (from-to)21-40
ISSN0213-8409
DOIs
Publication statusPublished - 2019

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meromictic lake
iron
mineral
sediment
acetate
early Earth
substrate
incubation
particle
oxidation
anoxic sediment
lake
lifestyle
slurry
marine environment
Precambrian
mud
water column
glass
methane

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Rotaru, Amelia-Elena ; Posth, Nicole ; Löscher, Carolin ; Miracle, Maria R. ; Vincence, Eduardo ; Cox, Raymond Pickett ; Thompson, Jennifer ; Poulton, Simon W. ; Thamdrup, Bo. / Interspecies interactions mediated by conductive minerals in the sediments of the iron rich meromictic Lake La Cruz, Spain. In: Limnetica. 2019 ; Vol. 38, No. 1. pp. 21-40.
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title = "Interspecies interactions mediated by conductive minerals in the sediments of the iron rich meromictic Lake La Cruz, Spain",
abstract = "Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. Here we show that conductive particles drove the metabolic coupling between electroactive microbial clades from this environment. The anoxic sediment of Lake La Cruz was rich in biogeochemically ‘reactive’ iron minerals, and harbored known electroactive species such as Geobacter and Methanothrix, in addition to groups not ever linked to an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed 2 to 4 times higher methanogenic activity, as compared to incubations with non-conductive glass beads or without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated above 8 mM depending on substrate (8 ± 0.6 to 11.7 ± 1.2 mM). Only by enabling syntrophic acetate oxidation with conductive minerals we could prevent acetate accumulation. Acetate oxidation conductively coupled to methanogenic activity had a stoichiometric recovery of 70{\%} and could be maintained in subsequent transfers if and only if amended with conductive particles. Mud-free enrichments without conductive particles ceased any metabolic activity after the second transfer. Conductive particles preserved a consortium of Youngiibacter-Methanothrix, whereas without conductive particles Youngiibacter spp. died off. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles inferring that minerals may have arbitrated the earliest interspecies associations",
keywords = "Conductive particles, Direct interspecies electron transfer, Geobacter, Granular activated carbon, Iron meromictic lake, Magnetite, Methanothrix, Mineral mediated syntrophy, Youngiibacter",
author = "Amelia-Elena Rotaru and Nicole Posth and Carolin L{\"o}scher and Miracle, {Maria R.} and Eduardo Vincence and Cox, {Raymond Pickett} and Jennifer Thompson and Poulton, {Simon W.} and Bo Thamdrup",
year = "2019",
doi = "10.23818/limn.38.10",
language = "English",
volume = "38",
pages = "21--40",
journal = "Limnetica",
issn = "0213-8409",
publisher = "Asociacion Iberica de Limnologia",
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}

Interspecies interactions mediated by conductive minerals in the sediments of the iron rich meromictic Lake La Cruz, Spain. / Rotaru, Amelia-Elena; Posth, Nicole; Löscher, Carolin; Miracle, Maria R.; Vincence, Eduardo; Cox, Raymond Pickett; Thompson, Jennifer; Poulton, Simon W.; Thamdrup, Bo.

In: Limnetica, Vol. 38, No. 1, 2019, p. 21-40.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Interspecies interactions mediated by conductive minerals in the sediments of the iron rich meromictic Lake La Cruz, Spain

AU - Rotaru, Amelia-Elena

AU - Posth, Nicole

AU - Löscher, Carolin

AU - Miracle, Maria R.

AU - Vincence, Eduardo

AU - Cox, Raymond Pickett

AU - Thompson, Jennifer

AU - Poulton, Simon W.

AU - Thamdrup, Bo

PY - 2019

Y1 - 2019

N2 - Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. Here we show that conductive particles drove the metabolic coupling between electroactive microbial clades from this environment. The anoxic sediment of Lake La Cruz was rich in biogeochemically ‘reactive’ iron minerals, and harbored known electroactive species such as Geobacter and Methanothrix, in addition to groups not ever linked to an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed 2 to 4 times higher methanogenic activity, as compared to incubations with non-conductive glass beads or without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated above 8 mM depending on substrate (8 ± 0.6 to 11.7 ± 1.2 mM). Only by enabling syntrophic acetate oxidation with conductive minerals we could prevent acetate accumulation. Acetate oxidation conductively coupled to methanogenic activity had a stoichiometric recovery of 70% and could be maintained in subsequent transfers if and only if amended with conductive particles. Mud-free enrichments without conductive particles ceased any metabolic activity after the second transfer. Conductive particles preserved a consortium of Youngiibacter-Methanothrix, whereas without conductive particles Youngiibacter spp. died off. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles inferring that minerals may have arbitrated the earliest interspecies associations

AB - Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. Here we show that conductive particles drove the metabolic coupling between electroactive microbial clades from this environment. The anoxic sediment of Lake La Cruz was rich in biogeochemically ‘reactive’ iron minerals, and harbored known electroactive species such as Geobacter and Methanothrix, in addition to groups not ever linked to an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed 2 to 4 times higher methanogenic activity, as compared to incubations with non-conductive glass beads or without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated above 8 mM depending on substrate (8 ± 0.6 to 11.7 ± 1.2 mM). Only by enabling syntrophic acetate oxidation with conductive minerals we could prevent acetate accumulation. Acetate oxidation conductively coupled to methanogenic activity had a stoichiometric recovery of 70% and could be maintained in subsequent transfers if and only if amended with conductive particles. Mud-free enrichments without conductive particles ceased any metabolic activity after the second transfer. Conductive particles preserved a consortium of Youngiibacter-Methanothrix, whereas without conductive particles Youngiibacter spp. died off. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles inferring that minerals may have arbitrated the earliest interspecies associations

KW - Conductive particles

KW - Direct interspecies electron transfer

KW - Geobacter

KW - Granular activated carbon

KW - Iron meromictic lake

KW - Magnetite

KW - Methanothrix

KW - Mineral mediated syntrophy

KW - Youngiibacter

U2 - 10.23818/limn.38.10

DO - 10.23818/limn.38.10

M3 - Journal article

VL - 38

SP - 21

EP - 40

JO - Limnetica

JF - Limnetica

SN - 0213-8409

IS - 1

ER -