Characterization of diverse bacteriohopanepolyols in a permanently stratified, hyper-euxinic lake

Molly D. O'Beirne; Robert Sparkes; Trinity L. Hamilton; Bart E. van Dongen; William P. Gilhooly; Josef P. Werne

doi:10.1016/j.orggeochem.2022.104431

Characterization of diverse bacteriohopanepolyols in a permanently stratified, hyper-euxinic lake

Molly D. O'Beirne, Robert Sparkes, Trinity L. Hamilton, Bart E. van Dongen, William P. Gilhooly, Josef P. Werne

Plant and Microbial Biology

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

2 Scopus citations

Abstract

Bacteriohopanepolyols (BHPs) are a diverse class of bacterial lipids that hold promise as biomarkers of specific microbes, microbial processes, and environmental conditions. BHPs have been characterized in a variety of terrestrial and aquatic environments, but less is known about their distribution and abundance in extreme environmental systems. In the present study, samples taken from the water column and upper sediments of the hyper-euxinic, meromictic Mahoney Lake (Canada) were analyzed for BHPs. Analyses show distinct BHP distributions within the oxic mixolimnion, the chemocline, and the euxinic monimolimnion. Bacteriohopanetetrol (BHT) and unsaturated BHT are the dominant BHPs found in the oxic mixolimnion and at the chemocline, whereas a novel BHP (tentatively identified as diunsaturated aminotriol) dominates the euxinic monimolimnion. Along with the novel BHP structure, composite BHPs (i.e., BHT-cyclitol ether and BHT-glucosamine) were observed in the euxinic monimolimnion and sediments, indicating their production by anaerobic bacteria. Complementary metagenomic analysis of genes involved in BHP biosynthesis (i.e., shc, hpnH, hpnO, hpnP, and hpnR) further revealed that BHPs in Mahoney Lake are most likely produced by bacteria belonging to Deltaproteobacteria, Chloroflexi, Planctomycetia, and Verrucomicrobia. The combined observations of BHP distribution and metagenomic analyses additionally indicate that 2- and 3-methyl BHTs are produced within the euxinic sediments in response to low oxygen and high osmotic concentrations, as opposed to being diagnostic biomarkers of cyanobacteria and aerobic metabolisms.

Original language	English (US)
Article number	104431
Journal	Organic Geochemistry
Volume	168
DOIs	https://doi.org/10.1016/j.orggeochem.2022.104431
State	Published - Jun 2022

Bibliographical note

Funding Information:
Our gratitude goes to Wendy Pope of BC Parks for her assistance with permitting (Permit #107419 to WPG) and boat access to Mahoney Lake. Sediment coring would not have been accomplished without the assistance of Arielle Woods, Sam Mark, Sophie Lehman, and Maria Gracia Bustamante Rosell (Pitt). Thanks also goes to Fotios Fouskas and Alice Bosco-Santos (IUPUI) who collected and provided water column sulfate and sulfide concentrations, Abigail Savage, Melissa Maher and Saule Akhmetkaliyeva (MMU) who acetylated and filtered BHP fractions, as well as Maira Guzman and the Analytical Services facility (MMU) for preparing and tuning the LC–MS. We are also appreciative of the thoughtful critiques of Dr. Ellen Hopmans and an anonymous reviewer which have greatly improved the manuscript. This work was supported by a National Science Foundation grant to JPW [EAR-1424170] and WPG [EAR-1424228], and funding from Manchester Metropolitan University to RS. An Andrew Mellon Predoctoral Fellowship and Henry Leighton Memorial Graduate Award provided research support to MDO.

Funding Information:
Our gratitude goes to Wendy Pope of BC Parks for her assistance with permitting (Permit #107419 to WPG) and boat access to Mahoney Lake. Sediment coring would not have been accomplished without the assistance of Arielle Woods, Sam Mark, Sophie Lehman, and Maria Gracia Bustamante Rosell (Pitt). Thanks also goes to Fotios Fouskas and Alice Bosco-Santos (IUPUI) who collected and provided water column sulfate and sulfide concentrations, Abigail Savage, Melissa Maher and Saule Akhmetkaliyeva (MMU) who acetylated and filtered BHP fractions, as well as Maira Guzman and the Analytical Services facility (MMU) for preparing and tuning the LC–MS. We are also appreciative of the thoughtful critiques of Dr. Ellen Hopmans and an anonymous reviewer which have greatly improved the manuscript. This work was supported by a National Science Foundation grant to JPW [EAR-1424170] and WPG [EAR-1424228], and funding from Manchester Metropolitan University to RS. An Andrew Mellon Predoctoral Fellowship and Henry Leighton Memorial Graduate Award provided research support to MDO.

Publisher Copyright:
© 2022 The Authors

Keywords

Aminotriol
Anaerobic bacteria
Bacteriohopanepolyols
Euxinia
Mahoney Lake
Methylated BHPs
Planctomycetes

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title = "Characterization of diverse bacteriohopanepolyols in a permanently stratified, hyper-euxinic lake",

abstract = "Bacteriohopanepolyols (BHPs) are a diverse class of bacterial lipids that hold promise as biomarkers of specific microbes, microbial processes, and environmental conditions. BHPs have been characterized in a variety of terrestrial and aquatic environments, but less is known about their distribution and abundance in extreme environmental systems. In the present study, samples taken from the water column and upper sediments of the hyper-euxinic, meromictic Mahoney Lake (Canada) were analyzed for BHPs. Analyses show distinct BHP distributions within the oxic mixolimnion, the chemocline, and the euxinic monimolimnion. Bacteriohopanetetrol (BHT) and unsaturated BHT are the dominant BHPs found in the oxic mixolimnion and at the chemocline, whereas a novel BHP (tentatively identified as diunsaturated aminotriol) dominates the euxinic monimolimnion. Along with the novel BHP structure, composite BHPs (i.e., BHT-cyclitol ether and BHT-glucosamine) were observed in the euxinic monimolimnion and sediments, indicating their production by anaerobic bacteria. Complementary metagenomic analysis of genes involved in BHP biosynthesis (i.e., shc, hpnH, hpnO, hpnP, and hpnR) further revealed that BHPs in Mahoney Lake are most likely produced by bacteria belonging to Deltaproteobacteria, Chloroflexi, Planctomycetia, and Verrucomicrobia. The combined observations of BHP distribution and metagenomic analyses additionally indicate that 2- and 3-methyl BHTs are produced within the euxinic sediments in response to low oxygen and high osmotic concentrations, as opposed to being diagnostic biomarkers of cyanobacteria and aerobic metabolisms.",

keywords = "Aminotriol, Anaerobic bacteria, Bacteriohopanepolyols, Euxinia, Mahoney Lake, Methylated BHPs, Planctomycetes",

author = "O'Beirne, {Molly D.} and Robert Sparkes and Hamilton, {Trinity L.} and {van Dongen}, {Bart E.} and Gilhooly, {William P.} and Werne, {Josef P.}",

note = "Funding Information: Our gratitude goes to Wendy Pope of BC Parks for her assistance with permitting (Permit #107419 to WPG) and boat access to Mahoney Lake. Sediment coring would not have been accomplished without the assistance of Arielle Woods, Sam Mark, Sophie Lehman, and Maria Gracia Bustamante Rosell (Pitt). Thanks also goes to Fotios Fouskas and Alice Bosco-Santos (IUPUI) who collected and provided water column sulfate and sulfide concentrations, Abigail Savage, Melissa Maher and Saule Akhmetkaliyeva (MMU) who acetylated and filtered BHP fractions, as well as Maira Guzman and the Analytical Services facility (MMU) for preparing and tuning the LC–MS. We are also appreciative of the thoughtful critiques of Dr. Ellen Hopmans and an anonymous reviewer which have greatly improved the manuscript. This work was supported by a National Science Foundation grant to JPW [EAR-1424170] and WPG [EAR-1424228], and funding from Manchester Metropolitan University to RS. An Andrew Mellon Predoctoral Fellowship and Henry Leighton Memorial Graduate Award provided research support to MDO. Funding Information: Our gratitude goes to Wendy Pope of BC Parks for her assistance with permitting (Permit #107419 to WPG) and boat access to Mahoney Lake. Sediment coring would not have been accomplished without the assistance of Arielle Woods, Sam Mark, Sophie Lehman, and Maria Gracia Bustamante Rosell (Pitt). Thanks also goes to Fotios Fouskas and Alice Bosco-Santos (IUPUI) who collected and provided water column sulfate and sulfide concentrations, Abigail Savage, Melissa Maher and Saule Akhmetkaliyeva (MMU) who acetylated and filtered BHP fractions, as well as Maira Guzman and the Analytical Services facility (MMU) for preparing and tuning the LC–MS. We are also appreciative of the thoughtful critiques of Dr. Ellen Hopmans and an anonymous reviewer which have greatly improved the manuscript. This work was supported by a National Science Foundation grant to JPW [EAR-1424170] and WPG [EAR-1424228], and funding from Manchester Metropolitan University to RS. An Andrew Mellon Predoctoral Fellowship and Henry Leighton Memorial Graduate Award provided research support to MDO. Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

month = jun,

doi = "10.1016/j.orggeochem.2022.104431",

language = "English (US)",

volume = "168",

journal = "Organic Geochemistry",

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TY - JOUR

T1 - Characterization of diverse bacteriohopanepolyols in a permanently stratified, hyper-euxinic lake

AU - O'Beirne, Molly D.

AU - Sparkes, Robert

AU - Hamilton, Trinity L.

AU - van Dongen, Bart E.

AU - Gilhooly, William P.

AU - Werne, Josef P.

N1 - Funding Information: Our gratitude goes to Wendy Pope of BC Parks for her assistance with permitting (Permit #107419 to WPG) and boat access to Mahoney Lake. Sediment coring would not have been accomplished without the assistance of Arielle Woods, Sam Mark, Sophie Lehman, and Maria Gracia Bustamante Rosell (Pitt). Thanks also goes to Fotios Fouskas and Alice Bosco-Santos (IUPUI) who collected and provided water column sulfate and sulfide concentrations, Abigail Savage, Melissa Maher and Saule Akhmetkaliyeva (MMU) who acetylated and filtered BHP fractions, as well as Maira Guzman and the Analytical Services facility (MMU) for preparing and tuning the LC–MS. We are also appreciative of the thoughtful critiques of Dr. Ellen Hopmans and an anonymous reviewer which have greatly improved the manuscript. This work was supported by a National Science Foundation grant to JPW [EAR-1424170] and WPG [EAR-1424228], and funding from Manchester Metropolitan University to RS. An Andrew Mellon Predoctoral Fellowship and Henry Leighton Memorial Graduate Award provided research support to MDO. Funding Information: Our gratitude goes to Wendy Pope of BC Parks for her assistance with permitting (Permit #107419 to WPG) and boat access to Mahoney Lake. Sediment coring would not have been accomplished without the assistance of Arielle Woods, Sam Mark, Sophie Lehman, and Maria Gracia Bustamante Rosell (Pitt). Thanks also goes to Fotios Fouskas and Alice Bosco-Santos (IUPUI) who collected and provided water column sulfate and sulfide concentrations, Abigail Savage, Melissa Maher and Saule Akhmetkaliyeva (MMU) who acetylated and filtered BHP fractions, as well as Maira Guzman and the Analytical Services facility (MMU) for preparing and tuning the LC–MS. We are also appreciative of the thoughtful critiques of Dr. Ellen Hopmans and an anonymous reviewer which have greatly improved the manuscript. This work was supported by a National Science Foundation grant to JPW [EAR-1424170] and WPG [EAR-1424228], and funding from Manchester Metropolitan University to RS. An Andrew Mellon Predoctoral Fellowship and Henry Leighton Memorial Graduate Award provided research support to MDO. Publisher Copyright: © 2022 The Authors

PY - 2022/6

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N2 - Bacteriohopanepolyols (BHPs) are a diverse class of bacterial lipids that hold promise as biomarkers of specific microbes, microbial processes, and environmental conditions. BHPs have been characterized in a variety of terrestrial and aquatic environments, but less is known about their distribution and abundance in extreme environmental systems. In the present study, samples taken from the water column and upper sediments of the hyper-euxinic, meromictic Mahoney Lake (Canada) were analyzed for BHPs. Analyses show distinct BHP distributions within the oxic mixolimnion, the chemocline, and the euxinic monimolimnion. Bacteriohopanetetrol (BHT) and unsaturated BHT are the dominant BHPs found in the oxic mixolimnion and at the chemocline, whereas a novel BHP (tentatively identified as diunsaturated aminotriol) dominates the euxinic monimolimnion. Along with the novel BHP structure, composite BHPs (i.e., BHT-cyclitol ether and BHT-glucosamine) were observed in the euxinic monimolimnion and sediments, indicating their production by anaerobic bacteria. Complementary metagenomic analysis of genes involved in BHP biosynthesis (i.e., shc, hpnH, hpnO, hpnP, and hpnR) further revealed that BHPs in Mahoney Lake are most likely produced by bacteria belonging to Deltaproteobacteria, Chloroflexi, Planctomycetia, and Verrucomicrobia. The combined observations of BHP distribution and metagenomic analyses additionally indicate that 2- and 3-methyl BHTs are produced within the euxinic sediments in response to low oxygen and high osmotic concentrations, as opposed to being diagnostic biomarkers of cyanobacteria and aerobic metabolisms.

AB - Bacteriohopanepolyols (BHPs) are a diverse class of bacterial lipids that hold promise as biomarkers of specific microbes, microbial processes, and environmental conditions. BHPs have been characterized in a variety of terrestrial and aquatic environments, but less is known about their distribution and abundance in extreme environmental systems. In the present study, samples taken from the water column and upper sediments of the hyper-euxinic, meromictic Mahoney Lake (Canada) were analyzed for BHPs. Analyses show distinct BHP distributions within the oxic mixolimnion, the chemocline, and the euxinic monimolimnion. Bacteriohopanetetrol (BHT) and unsaturated BHT are the dominant BHPs found in the oxic mixolimnion and at the chemocline, whereas a novel BHP (tentatively identified as diunsaturated aminotriol) dominates the euxinic monimolimnion. Along with the novel BHP structure, composite BHPs (i.e., BHT-cyclitol ether and BHT-glucosamine) were observed in the euxinic monimolimnion and sediments, indicating their production by anaerobic bacteria. Complementary metagenomic analysis of genes involved in BHP biosynthesis (i.e., shc, hpnH, hpnO, hpnP, and hpnR) further revealed that BHPs in Mahoney Lake are most likely produced by bacteria belonging to Deltaproteobacteria, Chloroflexi, Planctomycetia, and Verrucomicrobia. The combined observations of BHP distribution and metagenomic analyses additionally indicate that 2- and 3-methyl BHTs are produced within the euxinic sediments in response to low oxygen and high osmotic concentrations, as opposed to being diagnostic biomarkers of cyanobacteria and aerobic metabolisms.

KW - Aminotriol

KW - Anaerobic bacteria

KW - Bacteriohopanepolyols

KW - Euxinia

KW - Mahoney Lake

KW - Methylated BHPs

KW - Planctomycetes

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ER -

Characterization of diverse bacteriohopanepolyols in a permanently stratified, hyper-euxinic lake

Abstract

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Keywords

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