On the evolution and physiology of cable bacteria

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avisTidsskriftartikelForskningpeer review

Standard

On the evolution and physiology of cable bacteria. / Kjeldsen, Kasper U; Schreiber, Lars; Thorup, Casper A; Boesen, Thomas; Bjerg, Jesper T; Yang, Tingting; Dueholm, Morten S; Larsen, Steffen; Risgaard-Petersen, Nils; Nierychlo, Marta; Schmid, Markus; Bøggild, Andreas; van de Vossenberg, Jack; Geelhoed, Jeanine S; Meysman, Filip J R; Wagner, Michael; Nielsen, Per H; Nielsen, Lars Peter; Schramm, Andreas.

I: Proceedings of the National Academy of Sciences of the United States of America, Bind 116, Nr. 38, 17.09.2019, s. 19116-19125.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avisTidsskriftartikelForskningpeer review

Harvard

Kjeldsen, KU, Schreiber, L, Thorup, CA, Boesen, T, Bjerg, JT, Yang, T, Dueholm, MS, Larsen, S, Risgaard-Petersen, N, Nierychlo, M, Schmid, M, Bøggild, A, van de Vossenberg, J, Geelhoed, JS, Meysman, FJR, Wagner, M, Nielsen, PH, Nielsen, LP & Schramm, A 2019, 'On the evolution and physiology of cable bacteria', Proceedings of the National Academy of Sciences of the United States of America, bind 116, nr. 38, s. 19116-19125. https://doi.org/10.1073/pnas.1903514116

APA

Kjeldsen, K. U., Schreiber, L., Thorup, C. A., Boesen, T., Bjerg, J. T., Yang, T., Dueholm, M. S., Larsen, S., Risgaard-Petersen, N., Nierychlo, M., Schmid, M., Bøggild, A., van de Vossenberg, J., Geelhoed, J. S., Meysman, F. J. R., Wagner, M., Nielsen, P. H., Nielsen, L. P., & Schramm, A. (2019). On the evolution and physiology of cable bacteria. Proceedings of the National Academy of Sciences of the United States of America, 116(38), 19116-19125. https://doi.org/10.1073/pnas.1903514116

CBE

Kjeldsen KU, Schreiber L, Thorup CA, Boesen T, Bjerg JT, Yang T, Dueholm MS, Larsen S, Risgaard-Petersen N, Nierychlo M, Schmid M, Bøggild A, van de Vossenberg J, Geelhoed JS, Meysman FJR, Wagner M, Nielsen PH, Nielsen LP, Schramm A. 2019. On the evolution and physiology of cable bacteria. Proceedings of the National Academy of Sciences of the United States of America. 116(38):19116-19125. https://doi.org/10.1073/pnas.1903514116

MLA

Kjeldsen, Kasper U o.a.. "On the evolution and physiology of cable bacteria". Proceedings of the National Academy of Sciences of the United States of America. 2019, 116(38). 19116-19125. https://doi.org/10.1073/pnas.1903514116

Vancouver

Kjeldsen KU, Schreiber L, Thorup CA, Boesen T, Bjerg JT, Yang T o.a. On the evolution and physiology of cable bacteria. Proceedings of the National Academy of Sciences of the United States of America. 2019 sep 17;116(38):19116-19125. https://doi.org/10.1073/pnas.1903514116

Author

Kjeldsen, Kasper U ; Schreiber, Lars ; Thorup, Casper A ; Boesen, Thomas ; Bjerg, Jesper T ; Yang, Tingting ; Dueholm, Morten S ; Larsen, Steffen ; Risgaard-Petersen, Nils ; Nierychlo, Marta ; Schmid, Markus ; Bøggild, Andreas ; van de Vossenberg, Jack ; Geelhoed, Jeanine S ; Meysman, Filip J R ; Wagner, Michael ; Nielsen, Per H ; Nielsen, Lars Peter ; Schramm, Andreas. / On the evolution and physiology of cable bacteria. I: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Bind 116, Nr. 38. s. 19116-19125.

Bibtex

@article{8351c81206ea4120bca8df84498ed488,
title = "On the evolution and physiology of cable bacteria",
abstract = "Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genomics and metagenomics to retrieve draft genomes of 3 marine Candidatus Electrothrix and 1 freshwater Ca. Electronema species. These genomes contain >50% unknown genes but still share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few core genes lost and 212 unique genes (from 197 gene families) conserved among cable bacteria. Last common ancestor analysis indicates gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomics of a Ca. Electronema enrichment, the genomes suggest that cable bacteria oxidize sulfide by reversing the canonical sulfate reduction pathway and fix CO2 using the Wood-Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N2, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, yet-unidentified conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, whereas cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.",
keywords = "Cable bacteria, Electromicrobiology, Microbial evolution, Microbial genome, Microbial physiology",
author = "Kjeldsen, {Kasper U} and Lars Schreiber and Thorup, {Casper A} and Thomas Boesen and Bjerg, {Jesper T} and Tingting Yang and Dueholm, {Morten S} and Steffen Larsen and Nils Risgaard-Petersen and Marta Nierychlo and Markus Schmid and Andreas B{\o}ggild and {van de Vossenberg}, Jack and Geelhoed, {Jeanine S} and Meysman, {Filip J R} and Michael Wagner and Nielsen, {Per H} and Nielsen, {Lars Peter} and Andreas Schramm",
year = "2019",
month = sep,
day = "17",
doi = "10.1073/pnas.1903514116",
language = "English",
volume = "116",
pages = "19116--19125",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "The National Academy of Sciences of the United States of America",
number = "38",

}

RIS

TY - JOUR

T1 - On the evolution and physiology of cable bacteria

AU - Kjeldsen, Kasper U

AU - Schreiber, Lars

AU - Thorup, Casper A

AU - Boesen, Thomas

AU - Bjerg, Jesper T

AU - Yang, Tingting

AU - Dueholm, Morten S

AU - Larsen, Steffen

AU - Risgaard-Petersen, Nils

AU - Nierychlo, Marta

AU - Schmid, Markus

AU - Bøggild, Andreas

AU - van de Vossenberg, Jack

AU - Geelhoed, Jeanine S

AU - Meysman, Filip J R

AU - Wagner, Michael

AU - Nielsen, Per H

AU - Nielsen, Lars Peter

AU - Schramm, Andreas

PY - 2019/9/17

Y1 - 2019/9/17

N2 - Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genomics and metagenomics to retrieve draft genomes of 3 marine Candidatus Electrothrix and 1 freshwater Ca. Electronema species. These genomes contain >50% unknown genes but still share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few core genes lost and 212 unique genes (from 197 gene families) conserved among cable bacteria. Last common ancestor analysis indicates gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomics of a Ca. Electronema enrichment, the genomes suggest that cable bacteria oxidize sulfide by reversing the canonical sulfate reduction pathway and fix CO2 using the Wood-Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N2, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, yet-unidentified conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, whereas cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.

AB - Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genomics and metagenomics to retrieve draft genomes of 3 marine Candidatus Electrothrix and 1 freshwater Ca. Electronema species. These genomes contain >50% unknown genes but still share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few core genes lost and 212 unique genes (from 197 gene families) conserved among cable bacteria. Last common ancestor analysis indicates gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomics of a Ca. Electronema enrichment, the genomes suggest that cable bacteria oxidize sulfide by reversing the canonical sulfate reduction pathway and fix CO2 using the Wood-Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N2, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, yet-unidentified conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, whereas cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.

KW - Cable bacteria

KW - Electromicrobiology

KW - Microbial evolution

KW - Microbial genome

KW - Microbial physiology

U2 - 10.1073/pnas.1903514116

DO - 10.1073/pnas.1903514116

M3 - Journal article

C2 - 31427514

VL - 116

SP - 19116

EP - 19125

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 38

ER -