Why Orange Guaymas Basin Beggiatoa spp. Are Orange: Single-Filament-Genome-Enabled Identification of an Abundant Octaheme Cytochrome with Hydroxylamine Oxidase, Hydrazine Oxidase, and Nitrite Reductase Activities

MacGregor, Barbara J.; Biddle, Jennifer F.; Siebert, Jason R.; Staunton, Eric; Hegg, Eric L.; Matthysse, Ann G.; Teske, Andreas

doi:10.1128/aem.02538-12

Cited by 33 publications

(50 citation statements)

References 37 publications

(36 reference statements)

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“…Beggiatoaceae are also found in a variety of freshwater and hypersaline environments; of particular relevance to this paper, they form multispecies hypersaline microbial mats in Guerrero Negro (Baja California, Mexico) together with Cyanobacteria, Chloroflexi, Bacteroidetes, and a diversity of other bacteria and archaea (2,4). The near-complete genome sequence of a single orange Guaymas Basin vacuolate Beggiatoa ("Candidatus Maribeggiatoa") filament, referred to here as the BOGUAY sequence, was recently obtained (B. J. MacGregor, J. F. Biddle, C. Harbort, A. G. Matthysse, A. Teske, submitted for publication) (5). A complete genome for the freshwater Beggiatoa alba B18LD (NCBI project ID 62137) and partial genomes for two filaments (BgP and BgS) from Baltic Sea harbor sediment (6) are available for comparison.…”

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confidence: 99%

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

MacGregor

Biddle

Teske

2013

Appl Environ Microbiol

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The draft genome sequence of a single orange Beggiatoa ("Candidatus Maribeggiatoa") filament collected from a microbial mat at a hydrothermal site in Guaymas Basin (Gulf of California, Mexico) shows evidence of extensive genetic exchange with cyanobacteria, in particular for sensory and signal transduction genes. A putative homing endonuclease gene and group I intron within the 23S rRNA gene; several group II catalytic introns; GyrB and DnaE inteins, also encoding homing endonucleases; multiple copies of sequences similar to the fdxN excision elements XisH and XisI (required for heterocyst differentiation in some cyanobacteria); and multiple sequences related to an open reading frame (ORF) (00024_0693) of unknown function all have close non-Beggiatoaceae matches with cyanobacterial sequences. Sequences similar to the uncharacterized ORF and Xis elements are found in other Beggiatoaceae genomes, a variety of cyanobacteria, and a few phylogenetically dispersed pleiomorphic or filamentous bacteria. We speculate that elements shared among filamentous bacterial species may have been exchanged in microbial mats and that some of them may be involved in cell differentiation.

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Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

MacGregor

Biddle

Teske

2013

Appl Environ Microbiol

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“…This Beggiatoa protein, BOGUAY_0691, was found to have nitrite reductase, hydroxylamine oxidase, and hydrazine oxidase properties in vitro (42). Although its physiological role remains uncertain, MacGregor et al (41,42) argued that the latter two functions are unlikely and that BOGUAY_0691 probably serves as a nitrite reductase in vivo. Indeed, its expression under anoxic, sulfidic conditions in our incubation experiments is further evidence for its involvement in reductive rather than oxidative dissimilatory N metabolism.…”

Section: Observations Of Cold Seeps and Large Sulfur-oxidizing Bacteriamentioning

confidence: 99%

“…We identified Beggiatoaceae sequences with PhymmBL (40), using a confidence score cutoff of 0.65 (as determined by simulated taxonomic classification [see below; see also Fig. S1 in the supplemental material]) and a custom database amended with contigs from the following draft genomes: Beggiatoa alba B18LD (NCBI BioProject number 62137), "Beggiatoa orange Guaymas" (41,42), "Beggiatoa PS" and "Beggiatoa SS" (43), Thioploca araucae Tha-CCL (NCBI BioProject number 19383), and an unpublished Thiomargarita nelsonii genome. The taxonomic composition of the mRNA subset was determined by PhymmBL classification of a subset of 31 conserved universal phylogenetic marker genes (44).…”

Section: Methodsmentioning

confidence: 99%

“…Maribeggiatoa") (41,42). This Beggiatoa protein, BOGUAY_0691, was found to have nitrite reductase, hydroxylamine oxidase, and hydrazine oxidase properties in vitro (42). Although its physiological role remains uncertain, MacGregor et al (41,42) argued that the latter two functions are unlikely and that BOGUAY_0691 probably serves as a nitrite reductase in vivo.…”

Section: Observations Of Cold Seeps and Large Sulfur-oxidizing Bacteriamentioning

confidence: 99%

“…The two longest contigs in the Beggiatoaceae bin are most similar to a recently characterized octaheme cytochrome that was proposed to be involved in the reduction of nitrogenous compounds in vacuolated marine Beggiatoa ("Ca. Maribeggiatoa") (41,42). This Beggiatoa protein, BOGUAY_0691, was found to have nitrite reductase, hydroxylamine oxidase, and hydrazine oxidase properties in vitro (42).…”

Section: Observations Of Cold Seeps and Large Sulfur-oxidizing Bacteriamentioning

confidence: 99%

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Metatranscriptomic Analysis of Diminutive Thiomargarita-Like Bacteria (“Candidatus Thiopilula” spp.) from Abyssal Cold Seeps of the Barbados Accretionary Prism

Jones

Flood

Bailey

2015

Appl Environ Microbiol

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Large sulfur-oxidizing bacteria in the family Beggiatoaceae are important players in the global sulfur cycle. This group contains members of the well-known genera Beggiatoa, Thioploca, and Thiomargarita but also recently identified and relatively unknown candidate taxa, including "Candidatus Thiopilula" spp. and "Ca. Thiophysa" spp. We discovered a population of "Ca. Thiopilula" spp. colonizing cold seeps near Barbados at a ϳ4.7-km water depth. The Barbados population consists of spherical cells that are morphologically similar to Thiomargarita spp., with elemental sulfur inclusions and a central vacuole, but have much smaller cell diameters (5 to 40 m). Metatranscriptomic analysis revealed that when exposed to anoxic sulfidic conditions, Barbados "Ca. Thiopilula" organisms expressed genes for the oxidation of elemental sulfur and the reduction of nitrogenous compounds, consistent with their vacuolated morphology and intracellular sulfur storage capability. Metatranscriptomic analysis further revealed that anaerobic methane-oxidizing and sulfate-reducing organisms were active in the sediment, which likely provided reduced sulfur substrates for "Ca. Thiopilula" and other sulfur-oxidizing microorganisms in the community. The novel observations of "Ca. Thiopilula" and associated organisms reported here expand our knowledge of the globally distributed and ecologically successful Beggiatoaceae group and thus offer insight into the composition and ecology of deep cold seep microbial communities.T he family Beggiatoaceae contains the sulfur-oxidizing genera Beggiatoa, Thioploca, and Thiomargarita, including the largest known bacterium, Thiomargarita namibiensis, which can have cell diameters of Ͼ750 m (1, 2). Certain members of the Beggiatoaceae store nitrate in a large central vacuole, which supplies an electron acceptor to fuel anaerobic sulfur oxidation when oxygen is unavailable (2-4). As sulfide-oxidizing lithotrophs, members of the Beggiatoaceae thrive in diverse sulfidic environments (5, 6). Biomats constructed by these microorganisms are a conspicuous feature at oxygen minimum zones, hydrocarbon seeps, hydrothermal vents, and whale falls (see reference 7 and references therein), where they fill important roles in the global carbon and sulfur cycles. For example, the Beggiatoaceae are often primary producers in sulfidic marine sediments, where they act to conserve some of the potential energy present in sulfide that is produced during the anaerobic remineralization of organic carbon. As much as 80 to 95% of the sulfide produced during sulfate reduction escapes burial and is reoxidized, and much of this reoxidation occurs in the shallow sediment zone (8, 9). In addition to catalyzing important sulfur and nitrogen transformations, marine representatives of the Beggiatoaceae may even contribute to phosphate mineral formation (10-12). Furthermore, because of their large size and morphological complexity, Beggiatoa-and Thiomargarita-like cells have been identified in the fossil record and offer clues to microbial sul...

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Guaymas Basin, a Hydrothermal Hydrocarbon Seep Ecosystem

Teske

2020

Springer Oceanography

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Why Orange Guaymas Basin Beggiatoa spp. Are Orange: Single-Filament-Genome-Enabled Identification of an Abundant Octaheme Cytochrome with Hydroxylamine Oxidase, Hydrazine Oxidase, and Nitrite Reductase Activities

Cited by 33 publications

References 37 publications

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

Metatranscriptomic Analysis of Diminutive Thiomargarita-Like Bacteria (“Candidatus Thiopilula” spp.) from Abyssal Cold Seeps of the Barbados Accretionary Prism

Guaymas Basin, a Hydrothermal Hydrocarbon Seep Ecosystem

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