Phanerozoic radiation of ammonia oxidizing bacteria

Ward, Lewis M.; Johnston, David T.; Shih, Patrick M.

doi:10.1038/s41598-021-81718-2

Cited by 15 publications

(21 citation statements)

References 85 publications

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“…Angelarchaeales likely occur in a variety of soils and sediments where they have so far gone undetected using primer based CuMMO survey methods. Thus, this new clade of CuMMOs provides an opportunity for further study of these enzymes, and for molecular clock-based analyses of their evolution relative to Earth history [ 51 ].…”

Section: Discussionmentioning

confidence: 99%

Soils and sediments host Thermoplasmata archaea encoding novel copper membrane monooxygenases (CuMMOs)

et al. 2022

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Copper membrane monooxygenases (CuMMOs) play critical roles in the global carbon and nitrogen cycles. Organisms harboring these enzymes perform the first, and rate limiting, step in aerobic oxidation of ammonia, methane, or other simple hydrocarbons. Within archaea, only organisms in the order Nitrososphaerales (Thaumarchaeota) encode CuMMOs, which function exclusively as ammonia monooxygenases. From grassland and hillslope soils and aquifer sediments, we identified 20 genomes from distinct archaeal species encoding divergent CuMMO sequences. These archaea are phylogenetically clustered in a previously unnamed Thermoplasmatota order, herein named the Ca. Angelarchaeales. The CuMMO proteins in Ca. Angelarchaeales are more similar in structure to those in Nitrososphaerales than those of bacteria, and contain all functional residues required for general monooxygenase activity. Ca. Angelarchaeales genomes are significantly enriched in blue copper proteins (BCPs) relative to sibling lineages, including plastocyanin-like electron carriers and divergent nitrite reductase-like (nirK) 2-domain cupredoxin proteins co-located with electron transport machinery. Ca. Angelarchaeales also encode significant capacity for peptide/amino acid uptake and degradation and share numerous electron transport mechanisms with the Nitrososphaerales. Ca. Angelarchaeales are detected at high relative abundance in some of the environments where their genomes originated from. While the exact substrate specificities of the novel CuMMOs identified here have yet to be determined, activity on ammonia is possible given their metabolic and ecological context. The identification of an archaeal CuMMO outside of the Nitrososphaerales significantly expands the known diversity of CuMMO enzymes in archaea and suggests previously unaccounted organisms contribute to critical global nitrogen and/or carbon cycling functions.

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Section: Discussionmentioning

confidence: 99%

Soils and sediments host Thermoplasmata archaea encoding novel copper membrane monooxygenases (CuMMOs)

et al. 2022

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“…The antiquity of rTCA in NOB relative to Chlorobi is further consistent with the higher sequence-level diversity of rTCA proteins such as ATP citrate lyase in NOB (>75% similarity between sequences from Chlorobi, >65% between Nitrospirota, as low as ~53% between Nitrospinota), consistent with NOB having radiated over substantially longer evolutionary timescales than rTCA-encoding Chlorobi. This is possibility is supported by molecular clock studies that have placed the radiation of Nitrospirota and Nitrospinota >1.5 Gya [ 31 ].…”

Section: Resultsmentioning

confidence: 93%

“…Phylogenetic placement of Cyc2 Cytochromes from Chlorobi are in a fairly derived position, sister to a clade made up of iron oxidizing Betaproteobacteria such as Gallionella and Sideroxydans , nested within a broader radiation of proteobacterial sequences. Recent molecular clock estimates for the antiquity of Zeta- and Beta-proteobacteria suggest that these clades are less than ~1.8 Ga, with crown group Proteobacteria ~2.2 Ga [ 31 ]; together with our results here, this suggests that much if not all of the diversity of neutrophilic iron oxidizing bacteria that utilize Cyc2 Cytochrome homologs have radiated after the Great Oxygenation Event ~2.3 Gya when aerobic metabolisms first became viable due to the accumulation of significant atmospheric O 2 .…”

Section: Resultsmentioning

confidence: 99%

“…Taxonomic assignment was confirmed with GTDB-Tk [26][27][28]. Histories of vertical versus horizontal inheritance of metabolic proteins was made by comparison of organismal and metabolic protein phylogenies as described previously [29][30] Molecular clock analyses were performed following methods described briefly below, as established previously in [31,32]. A concatenated protein sequence alignment was generated by extracting and aligning protein sequences for marker genes followed by concatenation of aligned sequences.…”

Section: Methodsmentioning

confidence: 99%

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Phototrophy and carbon fixation in Chlorobi postdate the rise of oxygen

Ward

Shih²

2022

PLoS ONE

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While most productivity on the surface of the Earth today is fueled by oxygenic photosynthesis, for much of Earth history it is thought that anoxygenic photosynthesis—using compounds like ferrous iron or sulfide as electron donors—drove most global carbon fixation. Anoxygenic photosynthesis is still performed by diverse bacteria in niche environments today. Of these, the Chlorobi (formerly green sulfur bacteria) are often interpreted as being particularly ancient and are frequently proposed to have fueled the biosphere during late Archean and early Paleoproterozoic time before the rise of oxygenic photosynthesis. Here, we perform comparative genomic, phylogenetic, and molecular clock analyses to determine the antiquity of the Chlorobi and their characteristic phenotypes. We show that contrary to common assumptions, the Chlorobi clade is relatively young, with anoxygenic phototrophy, carbon fixation via the rTCA pathway, and iron oxidation all significantly postdating the rise of oxygen ~2.3 billion years ago. The Chlorobi therefore could not have fueled the Archean biosphere, but instead represent a relatively young radiation of organisms which likely acquired the capacity for anoxygenic photosynthesis and other traits via horizontal gene transfer sometime after the evolution of oxygenic Cyanobacteria.

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“…It can be found only in a limited number of bacteria and archaea. A recent phylogenomic analysis suggested that AOA originated from the terrestrial non-ammonia-oxidizing ancestors and expanded to the shallow and then deep ocean upon their oxygenation ( Ren et al, 2019 ), while ammonia-oxidizing bacteria are much younger ( Ward et al, 2021 ). Note however that this model is still under discussion ( Abby et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

(S)-3-Hydroxybutyryl-CoA Dehydrogenase From the Autotrophic 3-Hydroxypropionate/4-Hydroxybutyrate Cycle in Nitrosopumilus maritimus

et al. 2021

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Ammonia-oxidizing archaea of the phylum Thaumarchaeota are among the most abundant organisms that exert primary control of oceanic and soil nitrification and are responsible for a large part of dark ocean primary production. They assimilate inorganic carbon via an energetically efficient version of the 3-hydroxypropionate/4-hydroxybutyrate cycle. In this cycle, acetyl-CoA is carboxylated to succinyl-CoA, which is then converted to two acetyl-CoA molecules with 4-hydroxybutyrate as the key intermediate. This conversion includes the (S)-3-hydroxybutyryl-CoA dehydrogenase reaction. Here, we heterologously produced the protein Nmar_1028 catalyzing this reaction in thaumarchaeon Nitrosopumilus maritimus, characterized it biochemically and performed its phylogenetic analysis. This NAD-dependent dehydrogenase is highly active with its substrate, (S)-3-hydroxybutyryl-CoA, and its low Km value suggests that the protein is adapted to the functioning in the 3-hydroxypropionate/4-hydroxybutyrate cycle. Nmar_1028 is homologous to the dehydrogenase domain of crotonyl-CoA hydratase/(S)-3-hydroxybutyryl-CoA dehydrogenase that is present in many Archaea. Apparently, the loss of the dehydratase domain of the fusion protein in the course of evolution was accompanied by lateral gene transfer of 3-hydroxypropionyl-CoA dehydratase/crotonyl-CoA hydratase from Bacteria. Although (S)-3-hydroxybutyryl-CoA dehydrogenase studied here is neither unique nor characteristic for the HP/HB cycle, Nmar_1028 appears to be the only (S)-3-hydroxybutyryl-CoA dehydrogenase in N. maritimus and is thus essential for the functioning of the 3-hydroxypropionate/4-hydroxybutyrate cycle and for the biology of this important marine archaeon.

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Phanerozoic radiation of ammonia oxidizing bacteria

Cited by 15 publications

References 85 publications

Soils and sediments host Thermoplasmata archaea encoding novel copper membrane monooxygenases (CuMMOs)

Soils and sediments host Thermoplasmata archaea encoding novel copper membrane monooxygenases (CuMMOs)

Phototrophy and carbon fixation in Chlorobi postdate the rise of oxygen

(S)-3-Hydroxybutyryl-CoA Dehydrogenase From the Autotrophic 3-Hydroxypropionate/4-Hydroxybutyrate Cycle in Nitrosopumilus maritimus

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