An isolated chemolithoautotrophic ecosystem deduced from environmental isotopes: Ayyalon cave (Israel)

Amos Frumkin; Ariel D. Chipman; Israel Naaman

doi:10.3389/fevo.2022.1040385

An isolated chemolithoautotrophic ecosystem deduced from environmental isotopes: Ayyalon cave (Israel)

Amos Frumkin^*, Ariel D. Chipman, Israel Naaman

^*Corresponding author for this work

Department of Ecology, Evolution & Behavior (EEB)

Research output: Contribution to journal › Article › peer-review

Abstract

The stable isotopes composition of chemolithoautotrophic cave ecosystems is known to differ from epigenic caves. Here we show that in addition, dead carbon (devoid of ¹⁴C), is utilized and transferred throughout this ecosystem, rendering it unsuitable for radiocarbon dating. The connectivity of the Ayyalon Cave ecosystem with the surface is studied, along with its sources of energy and carbon, as well as the interconnections between its constituents. We use isotopic evidence to show that its ancient resilient ecosystem is based on an underground food web depending on rich biomass production by chemolithoautotrophic nutrient supplies, detached from surface photosynthesis. Carbon isotopic values indicate that: (1) the microbial biota use bicarbonate from the groundwater (23.34 pMC [% of modern carbon]) rather than the atmospheric CO₂ above the water (71.36 pMC); (2) the depleted ¹⁴C signal is transferred through the entire ecosystem, indicating that the ecosystem is well-adapted and based on the cave biofilm which is in turn based on groundwater-dissolved inorganic carbon. Incubation of Ayyalon biofilm with ¹⁴C-labelled bicarbonate indicates uptake of the radio-labeled bicarbonate by sulfur-oxidizing proteobacteria Beggiatoa, suggesting that these sulfur-oxidizing microorganisms use the water-dissolved inorganic carbon for chemolithoautotrophic carbon fixation. Organic matter in the cave is much lighter in its stable nitrogen and carbon isotopes compared with respective surface values, as expected in chemolithoautotrophic systems. This evidence may be applicative to subsurface voids of ancient Earth environments and extraterrestrial systems.

Original language	American English
Article number	1040385
Journal	Frontiers in Ecology and Evolution
Volume	10
DOIs	https://doi.org/10.3389/fevo.2022.1040385
State	Published - 26 Jan 2023

Bibliographical note

Funding Information:
The Israel Hydrological Service and Israel Nature and Parks Authority financed the study (grant #0321869).

Funding Information:
We are grateful for the following assistance: Elisabetta Boaretto of the Kimmel Center for Archaeological Science, Weizmann Institute of Science, helped with the laboratory analysis of Ayyalon carbon isotopes. Chanan Dimentman of the Hebrew University separated faunal samples and sent them for definition. Aharon Oren of the Hebrew University helped with the incubation of Ayyalon’s biofilm with radio-labeled 14C bicarbonate. Boaz Luz and Eugeni Barkan helped with C and N isotopic analysis. Ronen Ron of the Hebrew University performed the statistical analysis. Oren Kolodny and Efrat Gavish-Regev of the Hebrew University, Serban Sarbu of California State University and Amitai Cooper of Intel provided useful advice.

Publisher Copyright:
Copyright © 2023 Frumkin, Chipman and Naaman.

Keywords

arthropod adaptation
biofilm
cave ecosystem
chemolithoautotrophy
environmental isotopes
radiocarbon
stable isotopes
sulfidic cave

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10.3389/fevo.2022.1040385

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abstract = "The stable isotopes composition of chemolithoautotrophic cave ecosystems is known to differ from epigenic caves. Here we show that in addition, dead carbon (devoid of 14C), is utilized and transferred throughout this ecosystem, rendering it unsuitable for radiocarbon dating. The connectivity of the Ayyalon Cave ecosystem with the surface is studied, along with its sources of energy and carbon, as well as the interconnections between its constituents. We use isotopic evidence to show that its ancient resilient ecosystem is based on an underground food web depending on rich biomass production by chemolithoautotrophic nutrient supplies, detached from surface photosynthesis. Carbon isotopic values indicate that: (1) the microbial biota use bicarbonate from the groundwater (23.34 pMC [% of modern carbon]) rather than the atmospheric CO2 above the water (71.36 pMC); (2) the depleted 14C signal is transferred through the entire ecosystem, indicating that the ecosystem is well-adapted and based on the cave biofilm which is in turn based on groundwater-dissolved inorganic carbon. Incubation of Ayyalon biofilm with 14C-labelled bicarbonate indicates uptake of the radio-labeled bicarbonate by sulfur-oxidizing proteobacteria Beggiatoa, suggesting that these sulfur-oxidizing microorganisms use the water-dissolved inorganic carbon for chemolithoautotrophic carbon fixation. Organic matter in the cave is much lighter in its stable nitrogen and carbon isotopes compared with respective surface values, as expected in chemolithoautotrophic systems. This evidence may be applicative to subsurface voids of ancient Earth environments and extraterrestrial systems.",

keywords = "arthropod adaptation, biofilm, cave ecosystem, chemolithoautotrophy, environmental isotopes, radiocarbon, stable isotopes, sulfidic cave",

author = "Amos Frumkin and Chipman, {Ariel D.} and Israel Naaman",

note = "Funding Information: The Israel Hydrological Service and Israel Nature and Parks Authority financed the study (grant #0321869). Funding Information: We are grateful for the following assistance: Elisabetta Boaretto of the Kimmel Center for Archaeological Science, Weizmann Institute of Science, helped with the laboratory analysis of Ayyalon carbon isotopes. Chanan Dimentman of the Hebrew University separated faunal samples and sent them for definition. Aharon Oren of the Hebrew University helped with the incubation of Ayyalon{\textquoteright}s biofilm with radio-labeled 14C bicarbonate. Boaz Luz and Eugeni Barkan helped with C and N isotopic analysis. Ronen Ron of the Hebrew University performed the statistical analysis. Oren Kolodny and Efrat Gavish-Regev of the Hebrew University, Serban Sarbu of California State University and Amitai Cooper of Intel provided useful advice. Publisher Copyright: Copyright {\textcopyright} 2023 Frumkin, Chipman and Naaman.",

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doi = "10.3389/fevo.2022.1040385",

language = "American English",

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T1 - An isolated chemolithoautotrophic ecosystem deduced from environmental isotopes

T2 - Ayyalon cave (Israel)

AU - Frumkin, Amos

AU - Chipman, Ariel D.

AU - Naaman, Israel

N1 - Funding Information: The Israel Hydrological Service and Israel Nature and Parks Authority financed the study (grant #0321869). Funding Information: We are grateful for the following assistance: Elisabetta Boaretto of the Kimmel Center for Archaeological Science, Weizmann Institute of Science, helped with the laboratory analysis of Ayyalon carbon isotopes. Chanan Dimentman of the Hebrew University separated faunal samples and sent them for definition. Aharon Oren of the Hebrew University helped with the incubation of Ayyalon’s biofilm with radio-labeled 14C bicarbonate. Boaz Luz and Eugeni Barkan helped with C and N isotopic analysis. Ronen Ron of the Hebrew University performed the statistical analysis. Oren Kolodny and Efrat Gavish-Regev of the Hebrew University, Serban Sarbu of California State University and Amitai Cooper of Intel provided useful advice. Publisher Copyright: Copyright © 2023 Frumkin, Chipman and Naaman.

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N2 - The stable isotopes composition of chemolithoautotrophic cave ecosystems is known to differ from epigenic caves. Here we show that in addition, dead carbon (devoid of 14C), is utilized and transferred throughout this ecosystem, rendering it unsuitable for radiocarbon dating. The connectivity of the Ayyalon Cave ecosystem with the surface is studied, along with its sources of energy and carbon, as well as the interconnections between its constituents. We use isotopic evidence to show that its ancient resilient ecosystem is based on an underground food web depending on rich biomass production by chemolithoautotrophic nutrient supplies, detached from surface photosynthesis. Carbon isotopic values indicate that: (1) the microbial biota use bicarbonate from the groundwater (23.34 pMC [% of modern carbon]) rather than the atmospheric CO2 above the water (71.36 pMC); (2) the depleted 14C signal is transferred through the entire ecosystem, indicating that the ecosystem is well-adapted and based on the cave biofilm which is in turn based on groundwater-dissolved inorganic carbon. Incubation of Ayyalon biofilm with 14C-labelled bicarbonate indicates uptake of the radio-labeled bicarbonate by sulfur-oxidizing proteobacteria Beggiatoa, suggesting that these sulfur-oxidizing microorganisms use the water-dissolved inorganic carbon for chemolithoautotrophic carbon fixation. Organic matter in the cave is much lighter in its stable nitrogen and carbon isotopes compared with respective surface values, as expected in chemolithoautotrophic systems. This evidence may be applicative to subsurface voids of ancient Earth environments and extraterrestrial systems.

AB - The stable isotopes composition of chemolithoautotrophic cave ecosystems is known to differ from epigenic caves. Here we show that in addition, dead carbon (devoid of 14C), is utilized and transferred throughout this ecosystem, rendering it unsuitable for radiocarbon dating. The connectivity of the Ayyalon Cave ecosystem with the surface is studied, along with its sources of energy and carbon, as well as the interconnections between its constituents. We use isotopic evidence to show that its ancient resilient ecosystem is based on an underground food web depending on rich biomass production by chemolithoautotrophic nutrient supplies, detached from surface photosynthesis. Carbon isotopic values indicate that: (1) the microbial biota use bicarbonate from the groundwater (23.34 pMC [% of modern carbon]) rather than the atmospheric CO2 above the water (71.36 pMC); (2) the depleted 14C signal is transferred through the entire ecosystem, indicating that the ecosystem is well-adapted and based on the cave biofilm which is in turn based on groundwater-dissolved inorganic carbon. Incubation of Ayyalon biofilm with 14C-labelled bicarbonate indicates uptake of the radio-labeled bicarbonate by sulfur-oxidizing proteobacteria Beggiatoa, suggesting that these sulfur-oxidizing microorganisms use the water-dissolved inorganic carbon for chemolithoautotrophic carbon fixation. Organic matter in the cave is much lighter in its stable nitrogen and carbon isotopes compared with respective surface values, as expected in chemolithoautotrophic systems. This evidence may be applicative to subsurface voids of ancient Earth environments and extraterrestrial systems.

KW - arthropod adaptation

KW - biofilm

KW - cave ecosystem

KW - chemolithoautotrophy

KW - environmental isotopes

KW - radiocarbon

KW - stable isotopes

KW - sulfidic cave

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DO - 10.3389/fevo.2022.1040385

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JF - Frontiers in Ecology and Evolution

M1 - 1040385

ER -

An isolated chemolithoautotrophic ecosystem deduced from environmental isotopes: Ayyalon cave (Israel)

Abstract

Bibliographical note

Keywords

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