Expansion of the “Sodium World” through Evolutionary Time and Taxonomic Space

Kozlova, Maria I.; Bushmakin, I. M.; Belyaeva, Julia; Shalaeva, Daria N.; Dibrova, Daria V.; Cherepanov, Dmitry A.

doi:10.1134/s0006297920120056

Cited by 5 publications

(6 citation statements)

References 166 publications

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“…mtr genes coding for Na + ‐translocating methyl‐H4‐MPT:coenzyme M methyltransferase were predicted in the ANME‐1‐like (anaerobic methane oxidizing archaea) genome of this study, suggesting that a Na + pump was associated with the methanogen for energy conservation. A Na + ‐based bioenergetics and multiple mechanisms for cytoplasmic pH homeostasis maintenance are regarded as a dominant manner, the so‐called ‘sodium world’, in early life form and even before (Kozlova et al ., 2020). Our genomics analyses indicated the persistence of the ‘sodium world’ in the Manleluag serpentinizing ecosystem.…”

Section: Resultsmentioning

confidence: 99%

Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Wang

Baker

et al. 2022

Environ Microbiol Rep

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Reduced substrates produced by the serpentinization reaction under hydration of olivine may have fuelled biological processes on early Earth. To understand the adaptive strategies and carbon metabolism of the microbes in the serpentinizing ecosystems, we reconstructed 18 draft genomes representing dominant species of Omnitrophicaeota, Gammaproteobacteria and Methanobacteria from the Manleluag serpentinizing spring in Zambales, Philippines (hyperalkaline and rich in methane and hydrogen). Phylogenomics revealed that two genomes were affiliated with a candidate phylum NPL-UPA2 and the references of all our genomes were derived from ground waters, hot springs and the deep biosphere. C1 metabolism appears to be widespread as most of the genomes code for methanogenesis, CO oxidation and CO 2 fixation. However, likely due to the low CO 2 concentration and election acceptors, the biomass in the spring was extremely low (<10 3 cell/ml). Various Na + and K + transporters and Na + -driving ATPases appear to be encoded by these genomes, suggesting that nutrient acquisition, bioenergetics and normal cytoplasmic pH were dependent on Na + and K + pumps. Our results advance our understanding of the metabolic potentials and bioenergetics of serpentinizing springs and provide a framework of the ecology of early Earth.

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Section: Resultsmentioning

confidence: 99%

Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Wang

Baker

et al. 2022

Environ Microbiol Rep

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“…In fact, Na + energetics is considered to be the most ancient form of bioenergetics. Genomic analyses suggest that it is still prevalent throughout the tree of life today 18,30 .…”

Section: Discussionmentioning

confidence: 99%

“…As the first membranes were permeable to protons, the ion gradient was based on the impermeability of the membrane to sodium 18,29 . Accordingly, it has recently been shown that sodium-based bioenergetics is widespread throughout the tree of life (based on genome sampling for Na + -specific ATPases 30 ). Nevertheless, Na + energetics has not been much discussed in the cyanobacterial phyla, but see its role in cyanobacterial dormancy 20 .…”

Section: Sodium Energetics In Cyanobacteriamentioning

confidence: 99%

Unicellular cyanobacteria rely on sodium energetics to fix N₂

Tang,

Cheng,

Liu

et al. 2024

Preprint

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Diazotrophic cyanobacteria can thrive in combined nitrogen (N)-limited environments due to their ability to fix nitrogen gas (N2) from the atmosphere. Despite this, they occur in low abundance in N-limited coastal waters, which represents an ecological paradox1–3. One hypothesis is that this is partly due to elevated salinity (> 10 g/L NaCl), which inhibits cyanobacterial N2fixation2,3. Here we show that N2fixation in a unicellular coastal cyanobacterium is not inhibited but rather exclusively dependent on sodium (Na+) ions. In N-deficient environments, both N2fixation and population growth were significantly inhibited at low NaCl concentrations (< 4 g/L). Additional experiments indicated that sodium energetics, rather than proton energetics, is necessary for N2fixation, as Na+deficiency resulted in insufficient ATP supply for N2fixation. We show that this is due to the non-functioning Na+-coupled ATP synthase, which we found to be likely coupled to anaerobic rather than aerobic respiration. Sequence alignment analysis of the ion-coupling site of the ATP synthase revealed a high prevalence of Na+energetics in cyanobacteria, with all unicellular N2fixers capable of Na+energetics. This suggests a critical role for sodium energetics in cyanobacteria. It also raises the possibility that sodium energetics is not as rare as thought, but that we may have underestimated the prevalence and importance of sodium energetics in other organisms. Finally, the low abundance of diazotrophic unicellular cyanobacteria in coastal waters may be due to insufficient NaCl levels to support N2-fixation during periods of growth-supporting high temperatures. This provides another perspective on the regulation of the oceanic N cycle that needs to be considered in times of global climate change. Changes in current patterns could lead to an overlap of periods optimal for N2fixation and population growth, likely resulting in dense cyanobacterial blooms.

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“…NQR reductases operate as redox-driven sodium pumps, i.e., they generate a sodium ion motive force rather than PMF [28][29][30]. The sodium ion motive force, along with PMF and ATP, is the third energy currency used by a few bacteria [31]. Bacteria with more than one NADH:quinone reductase show a preference for one or another enzyme depending on the growth conditions.…”

Section: Bacterial Aerobic Respiratory Chainsmentioning

confidence: 99%

Bioenergetics and Reactive Nitrogen Species in Bacteria

Borisov

Forte

2022

IJMS

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The production of reactive nitrogen species (RNS) by the innate immune system is part of the host's defense against invading pathogenic bacteria. In this review, we summarize recent studies on the molecular basis of the effects of nitric oxide and peroxynitrite on microbial respiration and energy conservation. We discuss possible molecular mechanisms underlying RNS resistance in bacteria mediated by unique respiratory oxygen reductases, the mycobacterial bcc-aa3 supercomplex, and bd-type cytochromes. A complete picture of the impact of RNS on microbial bioenergetics is not yet available. However, this research area is developing very rapidly, and the knowledge gained should help us develop new methods of treating infectious diseases.

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Expansion of the “Sodium World” through Evolutionary Time and Taxonomic Space

Cited by 5 publications

References 166 publications

Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Unicellular cyanobacteria rely on sodium energetics to fix N₂

Bioenergetics and Reactive Nitrogen Species in Bacteria

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Expansion of the “Sodium World” through Evolutionary Time and Taxonomic Space

Cited by 5 publications

References 166 publications

Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Unicellular cyanobacteria rely on sodium energetics to fix N2

Bioenergetics and Reactive Nitrogen Species in Bacteria

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Unicellular cyanobacteria rely on sodium energetics to fix N₂