Ecological succession leads to chemosynthesis in mats colonizing wood in sea water

Kalenitchenko, Dimitri; Dupraz, Marlène; Bris, Nadine Le; Petetin, C.; Rose, Christophe; West, Nyree J.; Galand, Pierre E.

doi:10.1038/ismej.2016.12

Cited by 33 publications

(46 citation statements)

References 66 publications

(76 reference statements)

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“…The microbial mat samples were lysed, and wood core samples were powdered as described earlier (Kalenitchenko et al., , ). The cell lysate was then transferred to the Maxwell ® 16 Blood DNA Purification kit cartridge and processed automatically with the Maxwell ® 16 automated extractor (Promega, Fitchburg, MA, USA).…”

Section: Methodsmentioning

confidence: 99%

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Ultrarare marine microbes contribute to key sulphur‐related ecosystem functions

et al. 2018

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The description of a rare biosphere within microbial communities has created great interest because microbes play a fundamental role in the functioning of all ecosystems on earth. Despite recent progress in understanding the ecology of the rare biosphere, the concept itself is still discussed, and fundamental questions remain. Here, we target the seed bank compartment of the rare biosphere, assess the level of rarity at which micro-organisms are still able to colonize an ecosystem and investigate whether rare species are functionally redundant. Using an original experimental design where wood in aquaria was inoculated with increasingly diluted coastal seawater, we show that bacteria that represented as few as 0.00000002% of the cells in the environment (or 1 cell in 10 L of seawater) were still able to grow and play key roles within the ecosystem. Our experiment further showed that some bacteria can be replaced by others that have the potential to fulfil the same metabolic tasks. This finding suggests some functional redundancy within bacterial species. However, when ultrarare bacteria were progressively removed, productivity was reduced, and below a certain threshold some processes were lost, and the function of the ecosystem was altered. Overall the study shows that bacteria that are not detected by high-throughput sequencing approaches are nevertheless viable and able to colonize new ecosystems, suggesting the need to consider ultrarare microbes in the marine environment.

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Section: Methodsmentioning

confidence: 99%

“…The microbial mat samples were lysed, and wood core samples were powdered as described earlier (Kalenitchenko et al, , 2016.…”

Section: Dna Extraction and Sequencingmentioning

confidence: 99%

Ultrarare marine microbes contribute to key sulphur‐related ecosystem functions

et al. 2018

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“…These mats were composed by Arcobacter spp. and Thiomargarita spp., which are known to be first colonizer in microbial mats at dynamic sulfidic habitats (Schulz, 2006;Sievert et al, 2007;Girnth et al, 2011;Kalenitchenko et al, 2016). On the contrary, white mats are dominated by filament forming Beggiatoa spp.…”

Section: Methane-related Habitat Conditionsmentioning

confidence: 99%

Benthic Foraminifera in Arctic Methane Hydrate Bearing Sediments

et al. 2019

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“…Many deep-sea Campylobacterota grow attached to surfaces 29,61,62 , thus, a “ Ca. Thiobarba” ancestor might have colonized mussel gills prior to acquiring the CBB cycle.…”

Section: Main Textmentioning

confidence: 99%

Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria)

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et al. 2018

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36Although the majority of known autotrophs use the Calvin-Benson-Bassham (CBB) cycle for 37 carbon fixation, all currently described autotrophs from the Campylobacterota (previously 38 Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We 39 discovered campylobacterotal epibionts ("Candidatus Thiobarba") of deep-sea mussels that 40 have acquired a complete CBB cycle and lost key genes of the rTCA cycle. Intriguingly, the 41 phylogenies of campylobacterotal CBB genes suggest they were acquired in multiple 42 transfers from Gammaproteobacteria closely related to sulfur-oxidizing endosymbionts 43 associated with the mussels, as well as from Betaproteobacteria. We hypothesize that 44 "Ca. Thiobarba" switched from the rTCA to a fully functional CBB cycle during its evolution, 45 by acquiring genes from multiple sources, including co-occurring symbionts. We also found 46 key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be 47 more widespread in this phylum than previously known. Metatranscriptomics and 48 metaproteomics confirmed high expression of CBB cycle genes in mussel-associated 49 "Ca. Thiobarba". Direct stable isotope fingerprinting showed that "Ca. Thiobarba" has typical 50 CBB signatures, additional evidence that it uses this cycle for carbon fixation. Our discovery 51 calls into question current assumptions about the distribution of carbon fixation pathways 52 across the tree of life, and the interpretation of stable isotope measurements in the 53 environment. 54 55All life on earth is based on carbon fixation, and its molecular machinery is increasingly 56 becoming a focus of biotechnology and geo-engineering efforts due to its potential to 57 improve crop yields and sequester carbon dioxide from the atmosphere 1 . Seven carbon 58 fixation pathways have evolved in nature, and one purely synthetic pathway runs in vitro [2][3][4] . 59Of the six natural pathways, the Calvin-Benson-Bassham (CBB) cycle was the first 60 discovered, and is believed to be the most widespread 5-7 . The CBB cycle is used by a 61 diverse array of organisms throughout the tree of life, including plants and algae, 62 cyanobacteria, and autotrophic members of the Alpha-, Beta-and Gammaproteobacteria. Its 63 key enzyme, the ribulose bisphosphate carboxylase/oxygenase (RuBisCO) is thought to be 64 the most abundant, as well as one of the most ancient enzymes on Earth 8,9 . 65 The reductive tricarboxylic acid (rTCA) cycle was the second described carbon fixation 66 pathway 10 . In short, it is a reversal of the energy-generating and oxidative TCA cycle. Instead 67 of oxidizing acetyl-CoA and generating ATP and reducing equivalents, it reduces CO2 at the 68 expense of ATP and reducing equivalents 2,7,10 . Most of the enzymes are shared with the TCA 69 cycle, except for those that catalyze irreversible reactions in the TCA, such as citrate 70 synthase, which is catalyzed by ATP citrate lyase in the rTCA. However, given sufficiently 71 high reactant to product ratios and ...

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Ecological succession leads to chemosynthesis in mats colonizing wood in sea water

Cited by 33 publications

References 66 publications

Ultrarare marine microbes contribute to key sulphur‐related ecosystem functions

Ultrarare marine microbes contribute to key sulphur‐related ecosystem functions

Benthic Foraminifera in Arctic Methane Hydrate Bearing Sediments

Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria)

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