Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions

IntroductionThe Caspian Sea is the world’s largest landlocked saline lake which lies between Europe and Asia. This region is particularly known for its large-scale oil reserves, pipelines, and drilling activities, which have contributed to the environmental decline of this lake. In addition to pollu...

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Main Authors: Z. G. Griffiths, Andrew D. Putt, J. I. Miller, Maria Fernanda Campa, Dominique C. Joyner, O. Pelz, Nargiz Garajayeva, M. Ceccopieri, P. Gardinali, Terry C. Hazen
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Microbiomes
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/frmbi.2023.1270352/full
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author Z. G. Griffiths
Z. G. Griffiths
Andrew D. Putt
Andrew D. Putt
J. I. Miller
Maria Fernanda Campa
Maria Fernanda Campa
Dominique C. Joyner
Dominique C. Joyner
O. Pelz
Nargiz Garajayeva
M. Ceccopieri
P. Gardinali
Terry C. Hazen
Terry C. Hazen
Terry C. Hazen
Terry C. Hazen
author_facet Z. G. Griffiths
Z. G. Griffiths
Andrew D. Putt
Andrew D. Putt
J. I. Miller
Maria Fernanda Campa
Maria Fernanda Campa
Dominique C. Joyner
Dominique C. Joyner
O. Pelz
Nargiz Garajayeva
M. Ceccopieri
P. Gardinali
Terry C. Hazen
Terry C. Hazen
Terry C. Hazen
Terry C. Hazen
author_sort Z. G. Griffiths
collection DOAJ
description IntroductionThe Caspian Sea is the world’s largest landlocked saline lake which lies between Europe and Asia. This region is particularly known for its large-scale oil reserves, pipelines, and drilling activities, which have contributed to the environmental decline of this lake. In addition to pollution from the petroleum industry, drainage from various river basins brings an influx of residential, industrial, and agricultural effluents that induce eutrophication and hypoxic conditions in deeper, colder waters, creating an oxygen gradient. The temperature and oxygen stratification in this environment has presented a unique opportunity to investigate the potential of the biodegradative processes carried out by the indigenous microbial community. We believe these indigenous microbes possess different metabolic capabilities to degrade oil as they adapted to declining oxygen concentrations and temperatures with increasing depths over a prolonged period. Hence, community structure and composition will vary with depth.MethodsMicrocosms were set up to observe the indigenous microbial reaction after a 60 ppm native crude oil amendment over 115 days. Surface water microcosms were incubated at 28ºC and aerated while deep water microcosms were incubated at 8ºC under anaerobic conditions. These two environmental conditions represent the temperature and oxygen extremes along the gradient and were selected as we try to simulate the indigenous community’s response to this oil contamination. DNA was extracted and amplified from these microcosms and sequenced. Bioinformatic analysis was performed to track changes in the abundance of taxa present and biodiversity over different time points to show the progression of community structure.ResultsAll microcosms showed the presence of hydrocarbon-degrading phyla, whose presence is consistent with other reports from oil-enriched environments. However, distinct communities were observed in oxic versus hypoxic microcosms.ConclusionOrders of Bacteria related to sulfate and nitrogen cycling were found in hypoxic microcosms, indicating a possible mechanism for the anaerobic biodegradation of crude oil. GC-MS analysis of initial and final microcosms also provided evidence of degradation of hydrocarbon fractions in both warm, oxic and cold, hypoxic conditions.
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spelling doaj.art-4a8fc5b7959a47dca22547d8ada50ca02023-12-14T16:43:06ZengFrontiers Media S.A.Frontiers in Microbiomes2813-43382023-12-01210.3389/frmbi.2023.12703521270352Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditionsZ. G. Griffiths0Z. G. Griffiths1Andrew D. Putt2Andrew D. Putt3J. I. Miller4Maria Fernanda Campa5Maria Fernanda Campa6Dominique C. Joyner7Dominique C. Joyner8O. Pelz9Nargiz Garajayeva10M. Ceccopieri11P. Gardinali12Terry C. Hazen13Terry C. Hazen14Terry C. Hazen15Terry C. Hazen16Bredesen Center – Genome Science & Technology, University of Tennessee, Knoxville, TN, United StatesInstitute for a Secure and Sustainable Environment, University of Tennessee, Knoxville, TN, United StatesOak Ridge National Laboratory, Oak Ridge, TN, United StatesDepartment of Earth & Planetary Sciences, University of Tennessee, Knoxville, TN, United StatesOffice of Innovative Technologies, University of Tennessee, Knoxville, TN, United StatesBredesen Center – Genome Science & Technology, University of Tennessee, Knoxville, TN, United StatesDepartment of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN, United StatesOak Ridge National Laboratory, Oak Ridge, TN, United StatesDepartment of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN, United StatesRegulatory Compliance and Environment, BP AGT Region, Baku, AzerbaijanRegulatory Compliance and Environment, BP AGT Region, Baku, AzerbaijanEnvironmental Analysis Research Lab, Florida International University, Miami, FL, United StatesEnvironmental Analysis Research Lab, Florida International University, Miami, FL, United StatesBredesen Center – Genome Science & Technology, University of Tennessee, Knoxville, TN, United StatesInstitute for a Secure and Sustainable Environment, University of Tennessee, Knoxville, TN, United StatesOak Ridge National Laboratory, Oak Ridge, TN, United StatesDepartment of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN, United StatesIntroductionThe Caspian Sea is the world’s largest landlocked saline lake which lies between Europe and Asia. This region is particularly known for its large-scale oil reserves, pipelines, and drilling activities, which have contributed to the environmental decline of this lake. In addition to pollution from the petroleum industry, drainage from various river basins brings an influx of residential, industrial, and agricultural effluents that induce eutrophication and hypoxic conditions in deeper, colder waters, creating an oxygen gradient. The temperature and oxygen stratification in this environment has presented a unique opportunity to investigate the potential of the biodegradative processes carried out by the indigenous microbial community. We believe these indigenous microbes possess different metabolic capabilities to degrade oil as they adapted to declining oxygen concentrations and temperatures with increasing depths over a prolonged period. Hence, community structure and composition will vary with depth.MethodsMicrocosms were set up to observe the indigenous microbial reaction after a 60 ppm native crude oil amendment over 115 days. Surface water microcosms were incubated at 28ºC and aerated while deep water microcosms were incubated at 8ºC under anaerobic conditions. These two environmental conditions represent the temperature and oxygen extremes along the gradient and were selected as we try to simulate the indigenous community’s response to this oil contamination. DNA was extracted and amplified from these microcosms and sequenced. Bioinformatic analysis was performed to track changes in the abundance of taxa present and biodiversity over different time points to show the progression of community structure.ResultsAll microcosms showed the presence of hydrocarbon-degrading phyla, whose presence is consistent with other reports from oil-enriched environments. However, distinct communities were observed in oxic versus hypoxic microcosms.ConclusionOrders of Bacteria related to sulfate and nitrogen cycling were found in hypoxic microcosms, indicating a possible mechanism for the anaerobic biodegradation of crude oil. GC-MS analysis of initial and final microcosms also provided evidence of degradation of hydrocarbon fractions in both warm, oxic and cold, hypoxic conditions.https://www.frontiersin.org/articles/10.3389/frmbi.2023.1270352/fulloil biodegradationtemperatureoxichypoxicmarinehydrocarbons
spellingShingle Z. G. Griffiths
Z. G. Griffiths
Andrew D. Putt
Andrew D. Putt
J. I. Miller
Maria Fernanda Campa
Maria Fernanda Campa
Dominique C. Joyner
Dominique C. Joyner
O. Pelz
Nargiz Garajayeva
M. Ceccopieri
P. Gardinali
Terry C. Hazen
Terry C. Hazen
Terry C. Hazen
Terry C. Hazen
Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
Frontiers in Microbiomes
oil biodegradation
temperature
oxic
hypoxic
marine
hydrocarbons
title Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
title_full Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
title_fullStr Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
title_full_unstemmed Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
title_short Comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
title_sort comparing the response of the indigenous microbial community to crude oil amendment in oxic versus hypoxic conditions
topic oil biodegradation
temperature
oxic
hypoxic
marine
hydrocarbons
url https://www.frontiersin.org/articles/10.3389/frmbi.2023.1270352/full
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