“Candidatus Chlorobium masyuteum,” a Novel Photoferrotrophic Green Sulfur Bacterium Enriched From a Ferruginous Meromictic Lake

N. Lambrecht; Z. Stevenson; C.S. Sheik; M.A. Pronschinske; H. Tong; E.D. Swanner

doi:10.3389/fmicb.2021.695260

“Candidatus Chlorobium masyuteum,” a Novel Photoferrotrophic Green Sulfur Bacterium Enriched From a Ferruginous Meromictic Lake

N. Lambrecht, Z. Stevenson, C.S. Sheik, M.A. Pronschinske, H. Tong, E.D. Swanner

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

6 Scopus citations

Abstract

Anoxygenic phototrophic bacteria can be important primary producers in some meromictic lakes. Green sulfur bacteria (GSB) have been detected in ferruginous lakes, with some evidence that they are photosynthesizing using Fe(II) as an electron donor (i.e., photoferrotrophy). However, some photoferrotrophic GSB can also utilize reduced sulfur compounds, complicating the interpretation of Fe-dependent photosynthetic primary productivity. An enrichment (BLA1) from meromictic ferruginous Brownie Lake, Minnesota, United States, contains an Fe(II)-oxidizing GSB and a metabolically flexible putative Fe(III)-reducing anaerobe. “Candidatus Chlorobium masyuteum” grows photoautotrophically with Fe(II) and possesses the putative Fe(II) oxidase-encoding cyc2 gene also known from oxygen-dependent Fe(II)-oxidizing bacteria. It lacks genes for oxidation of reduced sulfur compounds. Its genome encodes for hydrogenases and a reverse TCA cycle that may allow it to utilize H2 and acetate as electron donors, an inference supported by the abundance of this organism when the enrichment was supplied by these substrates and light. The anaerobe “Candidatus Pseudopelobacter ferreus” is in low abundance (∼1%) in BLA1 and is a putative Fe(III)-reducing bacterium from the Geobacterales ord. nov. While “Ca. C. masyuteum” is closely related to the photoferrotrophs C. ferroooxidans strain KoFox and C. phaeoferrooxidans strain KB01, it is unique at the genomic level. The main light-harvesting molecule was identified as bacteriochlorophyll c with accessory carotenoids of the chlorobactene series. BLA1 optimally oxidizes Fe(II) at a pH of 6.8, and the rate of Fe(II) oxidation was 0.63 ± 0.069 mmol day–1, comparable to other photoferrotrophic GSB cultures or enrichments. Investigation of BLA1 expands the genetic basis for phototrophic Fe(II) oxidation by GSB and highlights the role these organisms may play in Fe(II) oxidation and carbon cycling in ferruginous lakes. © Copyright © 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.

Original language	English (US)
Article number	695260
Number of pages	17
Journal	Frontiers in Microbiology
Volume	12
DOIs	https://doi.org/10.3389/fmicb.2021.695260
State	Published - Jun 9 2021

Bibliographical note

Funding Information:
This work was sponsored by the National Science Foundation (NSF) collaborative research grant (EAR—1660691 to ES and EAR—1660761 to CS). This work was also supported by the National Aeronautics and Space Administration (NASA) Interdisciplinary Consortium for Astrobiology Research grant 80NSSC21K0592, Metal Utilization and Selection across Eons (MUSE).

Funding Information:
Chad Wittkop and Sergei Katsev helped to collect water samples. We acknowledge the W. M. Keck Metabolomics Research Laboratory (Office of Biotechnology, Iowa State University) for providing analytical instrumentation and we thank Lucas Showman for his assistance and support. Tracey Stewart at the Roy J. Carver High Resolution Microscopy Facility at Iowa State University facilitated TEM sample preparation and imaging. ?i??ka D?ta, Alexander Hall, and Aharon Oren assisted with developing the species epithets. The Minneapolis Parks and Recreation Board supplied permits to work at Brownie Lake. This manuscript was originally part of a dissertation accepted by Iowa State University and edited for publication. Funding. This work was sponsored by the National Science Foundation (NSF) collaborative research grant (EAR?1660691 to ES and EAR?1660761 to CS). This work was also supported by the National Aeronautics and Space Administration (NASA) Interdisciplinary Consortium for Astrobiology Research grant 80NSSC21K0592, Metal Utilization and Selection across Eons (MUSE).

Publisher Copyright:
© Copyright © 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.

Keywords

Brownie Lake
early Earth biogeochemistry
geomicrobiology
green sulfur bacterium
iron cycling
meromictic
photoferrotrophy
phototrophic Fe(II) oxidation

Continental Scientific Drilling Facility tags

SWAN

PubMed: MeSH publication types

Journal Article

Publisher link

10.3389/fmicb.2021.695260

https://www.scopus.com/inward/record.uri?eid=2-s2.0-85111110757&doi=10.3389%2ffmicb.2021.695260&partnerID=40&md5=a2277b603d041864ed344dd1d274b1a4

Find It

Find It at U of M Libraries

Cite this

@article{8999e43a031a41d3befae195497b42d6,

title = "“Candidatus Chlorobium masyuteum,” a Novel Photoferrotrophic Green Sulfur Bacterium Enriched From a Ferruginous Meromictic Lake",

abstract = "Anoxygenic phototrophic bacteria can be important primary producers in some meromictic lakes. Green sulfur bacteria (GSB) have been detected in ferruginous lakes, with some evidence that they are photosynthesizing using Fe(II) as an electron donor (i.e., photoferrotrophy). However, some photoferrotrophic GSB can also utilize reduced sulfur compounds, complicating the interpretation of Fe-dependent photosynthetic primary productivity. An enrichment (BLA1) from meromictic ferruginous Brownie Lake, Minnesota, United States, contains an Fe(II)-oxidizing GSB and a metabolically flexible putative Fe(III)-reducing anaerobe. “Candidatus Chlorobium masyuteum” grows photoautotrophically with Fe(II) and possesses the putative Fe(II) oxidase-encoding cyc2 gene also known from oxygen-dependent Fe(II)-oxidizing bacteria. It lacks genes for oxidation of reduced sulfur compounds. Its genome encodes for hydrogenases and a reverse TCA cycle that may allow it to utilize H2 and acetate as electron donors, an inference supported by the abundance of this organism when the enrichment was supplied by these substrates and light. The anaerobe “Candidatus Pseudopelobacter ferreus” is in low abundance (∼1%) in BLA1 and is a putative Fe(III)-reducing bacterium from the Geobacterales ord. nov. While “Ca. C. masyuteum” is closely related to the photoferrotrophs C. ferroooxidans strain KoFox and C. phaeoferrooxidans strain KB01, it is unique at the genomic level. The main light-harvesting molecule was identified as bacteriochlorophyll c with accessory carotenoids of the chlorobactene series. BLA1 optimally oxidizes Fe(II) at a pH of 6.8, and the rate of Fe(II) oxidation was 0.63 ± 0.069 mmol day–1, comparable to other photoferrotrophic GSB cultures or enrichments. Investigation of BLA1 expands the genetic basis for phototrophic Fe(II) oxidation by GSB and highlights the role these organisms may play in Fe(II) oxidation and carbon cycling in ferruginous lakes. {\textcopyright} Copyright {\textcopyright} 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.",

keywords = "Brownie Lake, early Earth biogeochemistry, geomicrobiology, green sulfur bacterium, iron cycling, meromictic, photoferrotrophy, phototrophic Fe(II) oxidation",

author = "N. Lambrecht and Z. Stevenson and C.S. Sheik and M.A. Pronschinske and H. Tong and E.D. Swanner",

note = "Funding Information: This work was sponsored by the National Science Foundation (NSF) collaborative research grant (EAR—1660691 to ES and EAR—1660761 to CS). This work was also supported by the National Aeronautics and Space Administration (NASA) Interdisciplinary Consortium for Astrobiology Research grant 80NSSC21K0592, Metal Utilization and Selection across Eons (MUSE). Funding Information: Chad Wittkop and Sergei Katsev helped to collect water samples. We acknowledge the W. M. Keck Metabolomics Research Laboratory (Office of Biotechnology, Iowa State University) for providing analytical instrumentation and we thank Lucas Showman for his assistance and support. Tracey Stewart at the Roy J. Carver High Resolution Microscopy Facility at Iowa State University facilitated TEM sample preparation and imaging. ?i??ka D?ta, Alexander Hall, and Aharon Oren assisted with developing the species epithets. The Minneapolis Parks and Recreation Board supplied permits to work at Brownie Lake. This manuscript was originally part of a dissertation accepted by Iowa State University and edited for publication. Funding. This work was sponsored by the National Science Foundation (NSF) collaborative research grant (EAR?1660691 to ES and EAR?1660761 to CS). This work was also supported by the National Aeronautics and Space Administration (NASA) Interdisciplinary Consortium for Astrobiology Research grant 80NSSC21K0592, Metal Utilization and Selection across Eons (MUSE). Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.",

year = "2021",

month = jun,

day = "9",

doi = "10.3389/fmicb.2021.695260",

language = "English (US)",

volume = "12",

journal = "Frontiers in Microbiology",

issn = "1664-302X",

publisher = "Frontiers Media S. A.",

}

TY - JOUR

T1 - “Candidatus Chlorobium masyuteum,” a Novel Photoferrotrophic Green Sulfur Bacterium Enriched From a Ferruginous Meromictic Lake

AU - Lambrecht, N.

AU - Stevenson, Z.

AU - Sheik, C.S.

AU - Pronschinske, M.A.

AU - Tong, H.

AU - Swanner, E.D.

N1 - Funding Information: This work was sponsored by the National Science Foundation (NSF) collaborative research grant (EAR—1660691 to ES and EAR—1660761 to CS). This work was also supported by the National Aeronautics and Space Administration (NASA) Interdisciplinary Consortium for Astrobiology Research grant 80NSSC21K0592, Metal Utilization and Selection across Eons (MUSE). Funding Information: Chad Wittkop and Sergei Katsev helped to collect water samples. We acknowledge the W. M. Keck Metabolomics Research Laboratory (Office of Biotechnology, Iowa State University) for providing analytical instrumentation and we thank Lucas Showman for his assistance and support. Tracey Stewart at the Roy J. Carver High Resolution Microscopy Facility at Iowa State University facilitated TEM sample preparation and imaging. ?i??ka D?ta, Alexander Hall, and Aharon Oren assisted with developing the species epithets. The Minneapolis Parks and Recreation Board supplied permits to work at Brownie Lake. This manuscript was originally part of a dissertation accepted by Iowa State University and edited for publication. Funding. This work was sponsored by the National Science Foundation (NSF) collaborative research grant (EAR?1660691 to ES and EAR?1660761 to CS). This work was also supported by the National Aeronautics and Space Administration (NASA) Interdisciplinary Consortium for Astrobiology Research grant 80NSSC21K0592, Metal Utilization and Selection across Eons (MUSE). Publisher Copyright: © Copyright © 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.

PY - 2021/6/9

Y1 - 2021/6/9

N2 - Anoxygenic phototrophic bacteria can be important primary producers in some meromictic lakes. Green sulfur bacteria (GSB) have been detected in ferruginous lakes, with some evidence that they are photosynthesizing using Fe(II) as an electron donor (i.e., photoferrotrophy). However, some photoferrotrophic GSB can also utilize reduced sulfur compounds, complicating the interpretation of Fe-dependent photosynthetic primary productivity. An enrichment (BLA1) from meromictic ferruginous Brownie Lake, Minnesota, United States, contains an Fe(II)-oxidizing GSB and a metabolically flexible putative Fe(III)-reducing anaerobe. “Candidatus Chlorobium masyuteum” grows photoautotrophically with Fe(II) and possesses the putative Fe(II) oxidase-encoding cyc2 gene also known from oxygen-dependent Fe(II)-oxidizing bacteria. It lacks genes for oxidation of reduced sulfur compounds. Its genome encodes for hydrogenases and a reverse TCA cycle that may allow it to utilize H2 and acetate as electron donors, an inference supported by the abundance of this organism when the enrichment was supplied by these substrates and light. The anaerobe “Candidatus Pseudopelobacter ferreus” is in low abundance (∼1%) in BLA1 and is a putative Fe(III)-reducing bacterium from the Geobacterales ord. nov. While “Ca. C. masyuteum” is closely related to the photoferrotrophs C. ferroooxidans strain KoFox and C. phaeoferrooxidans strain KB01, it is unique at the genomic level. The main light-harvesting molecule was identified as bacteriochlorophyll c with accessory carotenoids of the chlorobactene series. BLA1 optimally oxidizes Fe(II) at a pH of 6.8, and the rate of Fe(II) oxidation was 0.63 ± 0.069 mmol day–1, comparable to other photoferrotrophic GSB cultures or enrichments. Investigation of BLA1 expands the genetic basis for phototrophic Fe(II) oxidation by GSB and highlights the role these organisms may play in Fe(II) oxidation and carbon cycling in ferruginous lakes. © Copyright © 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.

AB - Anoxygenic phototrophic bacteria can be important primary producers in some meromictic lakes. Green sulfur bacteria (GSB) have been detected in ferruginous lakes, with some evidence that they are photosynthesizing using Fe(II) as an electron donor (i.e., photoferrotrophy). However, some photoferrotrophic GSB can also utilize reduced sulfur compounds, complicating the interpretation of Fe-dependent photosynthetic primary productivity. An enrichment (BLA1) from meromictic ferruginous Brownie Lake, Minnesota, United States, contains an Fe(II)-oxidizing GSB and a metabolically flexible putative Fe(III)-reducing anaerobe. “Candidatus Chlorobium masyuteum” grows photoautotrophically with Fe(II) and possesses the putative Fe(II) oxidase-encoding cyc2 gene also known from oxygen-dependent Fe(II)-oxidizing bacteria. It lacks genes for oxidation of reduced sulfur compounds. Its genome encodes for hydrogenases and a reverse TCA cycle that may allow it to utilize H2 and acetate as electron donors, an inference supported by the abundance of this organism when the enrichment was supplied by these substrates and light. The anaerobe “Candidatus Pseudopelobacter ferreus” is in low abundance (∼1%) in BLA1 and is a putative Fe(III)-reducing bacterium from the Geobacterales ord. nov. While “Ca. C. masyuteum” is closely related to the photoferrotrophs C. ferroooxidans strain KoFox and C. phaeoferrooxidans strain KB01, it is unique at the genomic level. The main light-harvesting molecule was identified as bacteriochlorophyll c with accessory carotenoids of the chlorobactene series. BLA1 optimally oxidizes Fe(II) at a pH of 6.8, and the rate of Fe(II) oxidation was 0.63 ± 0.069 mmol day–1, comparable to other photoferrotrophic GSB cultures or enrichments. Investigation of BLA1 expands the genetic basis for phototrophic Fe(II) oxidation by GSB and highlights the role these organisms may play in Fe(II) oxidation and carbon cycling in ferruginous lakes. © Copyright © 2021 Lambrecht, Stevenson, Sheik, Pronschinske, Tong and Swanner.

KW - Brownie Lake

KW - early Earth biogeochemistry

KW - geomicrobiology

KW - green sulfur bacterium

KW - iron cycling

KW - meromictic

KW - photoferrotrophy

KW - phototrophic Fe(II) oxidation

U2 - 10.3389/fmicb.2021.695260

DO - 10.3389/fmicb.2021.695260

M3 - Article

C2 - 34305861

SN - 1664-302X

VL - 12

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

M1 - 695260

ER -

“Candidatus Chlorobium masyuteum,” a Novel Photoferrotrophic Green Sulfur Bacterium Enriched From a Ferruginous Meromictic Lake

Abstract

Bibliographical note

Keywords

Continental Scientific Drilling Facility tags

PubMed: MeSH publication types

Publisher link

Find It

Fingerprint

Cite this