Sulfide oxidation, nitrate respiration, carbon acquisition, and electron transport pathways suggested by the draft genome of a single orange Guaymas Basin Beggiatoa (Cand. Maribeggiatoa) sp. filament

Barbara J. MacGregor; Jennifer F. Biddle; Christopher Harbort; Ann G. Matthysse; Andreas Teske

doi:10.1016/j.margen.2013.08.001

Sulfide oxidation, nitrate respiration, carbon acquisition, and electron transport pathways suggested by the draft genome of a single orange Guaymas Basin Beggiatoa (Cand. Maribeggiatoa) sp. filament

Barbara J. MacGregor, Jennifer F. Biddle, Christopher Harbort, Ann G. Matthysse, Andreas Teske

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

25 Scopus citations

Abstract

A near-complete draft genome has been obtained for a single vacuolated orange Beggiatoa (Cand. Maribeggiatoa) filament from a Guaymas Basin seafloor microbial mat, the third relatively complete sequence for the Beggiatoaceae. Possible pathways for sulfide oxidation; nitrate respiration; inorganic carbon fixation by both Type II RuBisCO and the reductive tricarboxylic acid cycle; acetate and possibly formate uptake; and energy-generating electron transport via both oxidative phosphorylation and the Rnf complex are discussed here. A role in nitrite reduction is suggested for an abundant orange cytochrome produced by the Guaymas strain; this has a possible homolog in Beggiatoa (Cand. Isobeggiatoa) sp. PS, isolated from marine harbor sediment, but not Beggiatoa alba B18LD, isolated from a freshwater rice field ditch. Inferred phylogenies for the Calvin-Benson-Bassham (CBB) cycle and the reductive (rTCA) and oxidative (TCA) tricarboxylic acid cycles suggest that genes encoding succinate dehydrogenase and enzymes for carboxylation and/or decarboxylation steps (including RuBisCO) may have been introduced to (or exported from) one or more of the three genomes by horizontal transfer, sometimes by different routes. Sequences from the two marine strains are generally more similar to each other than to sequences from the freshwater strain, except in the case of RuBisCO: only the Guaymas strain encodes a Type II enzyme, which (where studied) discriminates less against oxygen than do Type I RuBisCOs. Genes subject to horizontal transfer may represent key steps for adaptation to factors such as oxygen and carbon dioxide concentration, organic carbon availability, and environmental variability.

Original language	English (US)
Pages (from-to)	53-65
Number of pages	13
Journal	Marine Genomics
Volume	11
DOIs	https://doi.org/10.1016/j.margen.2013.08.001
State	Published - Sep 2013
Externally published	Yes

Bibliographical note

Funding Information:
Thanks to the Captain and crews of the RV Atlantis and HOV Alvin , and to the shipboard parties of legs AT 15-40 and AT 15-56. Genome sequencing was performed by the J. Craig Venter Institute, with funding from The Gordon and Betty Moore Foundation Marine Microbial Genome Sequencing Project . The students and auditors of Dr. Ann Matthysse's 2010 and 2011 Bacterial Genetics (Biology 522) classes, Sarah Allen, Anke Dopychai, Paul Richard Dunbar, Stuart Hoyle, Stephanie Lambeth, Alex Lawler, Nicholas Panchy, Nikolas Stasulli, Lisa Nigro, Lindsay D'Ambrosio, Luke McKay, and TingTing Yang, helped with genome annotation; particular thanks is due to Elizabeth Littauer for her work on the TCA cycle. The use of RAST was supported in part by National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services (NIAD) under contract HHSN266200400042C . The Guaymas Basin project was funded by NSF OCE 0647633 .

Keywords

Hybrid cluster protein
ONR
Octaheme cytochrome
RTCA
RuBisCO
TCA

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Sulfide oxidation, nitrate respiration, carbon acquisition, and electron transport pathways suggested by the draft genome of a single orange Guaymas Basin Beggiatoa (Cand. Maribeggiatoa) sp. filament. / MacGregor, Barbara J.; Biddle, Jennifer F.; Harbort, Christopher et al.
In: Marine Genomics, Vol. 11, 09.2013, p. 53-65.

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

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abstract = "A near-complete draft genome has been obtained for a single vacuolated orange Beggiatoa (Cand. Maribeggiatoa) filament from a Guaymas Basin seafloor microbial mat, the third relatively complete sequence for the Beggiatoaceae. Possible pathways for sulfide oxidation; nitrate respiration; inorganic carbon fixation by both Type II RuBisCO and the reductive tricarboxylic acid cycle; acetate and possibly formate uptake; and energy-generating electron transport via both oxidative phosphorylation and the Rnf complex are discussed here. A role in nitrite reduction is suggested for an abundant orange cytochrome produced by the Guaymas strain; this has a possible homolog in Beggiatoa (Cand. Isobeggiatoa) sp. PS, isolated from marine harbor sediment, but not Beggiatoa alba B18LD, isolated from a freshwater rice field ditch. Inferred phylogenies for the Calvin-Benson-Bassham (CBB) cycle and the reductive (rTCA) and oxidative (TCA) tricarboxylic acid cycles suggest that genes encoding succinate dehydrogenase and enzymes for carboxylation and/or decarboxylation steps (including RuBisCO) may have been introduced to (or exported from) one or more of the three genomes by horizontal transfer, sometimes by different routes. Sequences from the two marine strains are generally more similar to each other than to sequences from the freshwater strain, except in the case of RuBisCO: only the Guaymas strain encodes a Type II enzyme, which (where studied) discriminates less against oxygen than do Type I RuBisCOs. Genes subject to horizontal transfer may represent key steps for adaptation to factors such as oxygen and carbon dioxide concentration, organic carbon availability, and environmental variability.",

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note = "Funding Information: Thanks to the Captain and crews of the RV Atlantis and HOV Alvin , and to the shipboard parties of legs AT 15-40 and AT 15-56. Genome sequencing was performed by the J. Craig Venter Institute, with funding from The Gordon and Betty Moore Foundation Marine Microbial Genome Sequencing Project . The students and auditors of Dr. Ann Matthysse's 2010 and 2011 Bacterial Genetics (Biology 522) classes, Sarah Allen, Anke Dopychai, Paul Richard Dunbar, Stuart Hoyle, Stephanie Lambeth, Alex Lawler, Nicholas Panchy, Nikolas Stasulli, Lisa Nigro, Lindsay D'Ambrosio, Luke McKay, and TingTing Yang, helped with genome annotation; particular thanks is due to Elizabeth Littauer for her work on the TCA cycle. The use of RAST was supported in part by National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services (NIAD) under contract HHSN266200400042C . The Guaymas Basin project was funded by NSF OCE 0647633 . ",

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Sulfide oxidation, nitrate respiration, carbon acquisition, and electron transport pathways suggested by the draft genome of a single orange Guaymas Basin Beggiatoa (Cand. Maribeggiatoa) sp. filament

Abstract

Bibliographical note

Keywords

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