<i>Candidatus</i> Thiovulum sp. strain imperiosus: the largest free-living Epsilonproteobacteraeota <i>Thiovulum</i> strain lives in a marine mangrove environment

Sylvestre, Marie-Noëlle; Jean-Louis, Patrick; Grimonprez, Adrien; Bilas, Philippe; Collienne, Amandine; Azède, Catherine; Gros, Olivier

doi:10.1139/cjm-2021-0101

Cited by 4 publications

(11 citation statements)

References 76 publications

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“…T. karukerense [ 26 ] and Ca . T. imperiosus [ 2 ] were respectively obtained from veils developing above the sediment and on bones deployed in marine mangrove in Guadeloupe (Lesser Antilles). Samples were collected manually between March and May 2021 in ~1 m depth (16°16'32.7“N 61°33'28.5“W).…”

Section: Methodsmentioning

confidence: 99%

“…While dense veils of Ca . T. karukerense naturally form above the mangrove sediment throughout the year, we had to deploy cleaned pig bones as described before [ 2 ] to collect live Ca . T. imperiosus individuals.…”

Section: Methodsmentioning

confidence: 99%

“…Thiovulum spp. are spherical bacteria typically <25 µm in diameter [ 1 ], but some can reach up to 50 µm [ 2 ]. Thiovulum spp.…”

Section: Introductionmentioning

confidence: 99%

“…we assembled from public data to their marine counterparts, including the genomes of Candidatus Thiovulum karukerense [ 26 ] and Ca . T. imperiosus [ 2 ], whose genomes are also presented here.

Fig.…”

Section: Introductionmentioning

confidence: 99%

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Cave Thiovulum (Candidatus Thiovulum stygium) differs metabolically and genomically from marine species

et al. 2022

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Thiovulum spp. (Campylobacterota) are large sulfur bacteria that form veil-like structures in aquatic environments. The sulfidic Movile Cave (Romania), sealed from the atmosphere for ~5 million years, has several aqueous chambers, some with low atmospheric O2 (~7%). The cave’s surface-water microbial community is dominated by bacteria we identified as Thiovulum. We show that this strain, and others from subsurface environments, are phylogenetically distinct from marine Thiovulum. We assembled a closed genome of the Movile strain and confirmed its metabolism using RNAseq. We compared the genome of this strain and one we assembled from public data from the sulfidic Frasassi caves to four marine genomes, including Candidatus Thiovulum karukerense and Ca. T. imperiosus, whose genomes we sequenced. Despite great spatial and temporal separation, the genomes of the Movile and Frasassi Thiovulum were highly similar, differing greatly from the very diverse marine strains. We concluded that cave Thiovulum represent a new species, named here Candidatus Thiovulum stygium. Based on their genomes, cave Thiovulum can switch between aerobic and anaerobic sulfide oxidation using O2 and NO3- as electron acceptors, the latter likely via dissimilatory nitrate reduction to ammonia. Thus, Thiovulum is likely important to both S and N cycles in sulfidic caves. Electron microscopy analysis suggests that at least some of the short peritrichous structures typical of Thiovulum are type IV pili, for which genes were found in all strains. These pili may play a role in veil formation, by connecting adjacent cells, and in the motility of these exceptionally fast swimmers.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

“…Thiovulum spp. are spherical bacteria typically <25 µm in diameter [ 1 ], but some can reach up to 50 µm [ 2 ]. Thiovulum spp.…”

Section: Introductionmentioning

confidence: 99%

“…we assembled from public data to their marine counterparts, including the genomes of Candidatus Thiovulum karukerense [ 26 ] and Ca . T. imperiosus [ 2 ], whose genomes are also presented here.

Fig.…”

Section: Introductionmentioning

confidence: 99%

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Cave Thiovulum (Candidatus Thiovulum stygium) differs metabolically and genomically from marine species

et al. 2022

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“…Thiovulum is a large bacterium, typically < 25 µm in diameter (Robertson et al, 2015) but can reach 45 µm (Sylvestre et al, 2021). It is a sulfur-oxidizing chemolithoautotrophic bacteria (Wirsen and Jannasch, 1978) with an extremely fast motility (Garcia-Pichel, 1989;Thar and Fenchel, 2001).…”

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confidence: 99%

CaveThiovulaceaediffer metabolically and genomically from marine species

Bižić

Brad

Barbu–Tudoran

et al. 2020

Preprint

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Life in Movile Cave (Romania) relies entirely on primary carbon fixation by bacteria oxidizing sulfide, methane and ammonia with oxygen, nitrate, sulfate, and ferric iron. There, large spherical-ovoid bacteria (12-16 µm diameter), rich in intracellular sulfur globules, dominate the stable microbial community in the surface water of a hypoxic Air Bell. These were identified as Thiovulum sp. (Campylobacterota). We obtained a closed genome of this Thiovulum and compared it to that of Thiovulum ES. The genes for oxidizing sulfide to sulfate are absent, therefore, Thiovulum likely avoids constant accumulation of elemental sulfur either by oxidizing sulfide to sulfite which is then excreted, or via dissimilatory nitrate reduction to ammonia using the formate-dependent nitrite reductase or hydroxylamine oxidoreductase. Thus, Thiovulum, found also in other caves, is likely important to both S and N cycles in subterranean aquatic ecosystems. Additionally, using electron microscopy, we suggest that in absence of motor-like structures along the membrane, the peritrichous flagella-like structures are type IV pili, for which genes were found in both Thiovulum genomes. These pili may play a role in veil formation, connecting adjacent cells. The force exerted by coordinated movement of such pili may partly explain the exceptionally fast swimming of these bacteria.

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Genomic Mysteries of Giant Bacteria: Insights and Implications

Ionescu,

Volland,

Contarini

et al. 2023

Genome Biology and Evolution

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Bacteria and Archaea are traditionally regarded as organisms with a simple morphology constrained to a size of 2-3 micrometers. Nevertheless, the history of microbial research is rich in description of giant bacteria exceeding tens, and even hundreds of micrometers in length or diameter already from its early days, e.g. Beggiatoa spp, to the present, e.g. Ca. Thiomargarita magnifica. While some of these giants are still being studied, some were lost to science, with merely drawing and photomicrographs as evidence for their existence. The physiology and biogeochemical role of giant bacteria has been studied, with a large focus on those involved in the sulfur cycle. With the onset of the genomic era, no special emphasis has been given to this group, in an attempt to gain a novel, evolutionary and molecular, understanding of the phenomenon of bacterial gigantism. The few existing genomic studies reveal a mysterious world of hyper-polyploid bacteria with hundreds to hundreds-of-thousands of chromosomes which are in some cases identical and in others, extremely different. These studies on giant bacteria reveal novel organelles, cellular compartmentalization, and novel mechanisms to combat the accumulation of deleterious mutation in polyploid bacteria. In this perspective paper, we provide a brief overview of what is known on the genomics of giant bacteria and build on that to highlight a few burning questions that await to be addressed.

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Candidatus Thiovulum sp. strain imperiosus: the largest free-living Epsilonproteobacteraeota Thiovulum strain lives in a marine mangrove environment

Cited by 4 publications

References 76 publications

Cave Thiovulum (Candidatus Thiovulum stygium) differs metabolically and genomically from marine species

Cave Thiovulum (Candidatus Thiovulum stygium) differs metabolically and genomically from marine species

CaveThiovulaceaediffer metabolically and genomically from marine species

Genomic Mysteries of Giant Bacteria: Insights and Implications

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