Purple sulfur bacteria fix N2 via molybdenum-nitrogenase in a low molybdenum Proterozoic ocean analogue

Philippi, Miriam; Kitzinger, Katharina; Berg, Jerry S. Vande; Tschitschko, Bernhard; Kidane, Abiel T.; Littmann, Sten; Marchant, Hannah K.; Storelli, Nicola; Winkel, Lenny H. E.; Schubert, Carsten J.; Mohr, Wiebke; Kuypers, Marcel M. M.

doi:10.1038/s41467-021-25000-z

Cited by 27 publications

(26 citation statements)

References 100 publications

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“…Under the archaea-first hypothesis, the six- nif- gene set first evolved in archaea, so it should be associated more often with wtpABC than with modABC , but the opposite is true in both archaea and bacteria. A recent study suggested that purple sulfur bacteria (Proteobacteria) could fix nitrogen and used ModABC transporter as early as 2.5–0.5 Ga ( Philippi et al 2021 ). As purple sulfur bacteria are not the oldest Nif species (Group I), there could be even older Nif bacteria that carried the modABC genes.…”

Section: Resultsmentioning

confidence: 99%

“…However, nitrogen-fixing (Nif) bacteria are physiologically and ecologically diverse. Most of them are free-living, including aerobic chemoorganotrophs ( Setubal et al 2009 ); anoxygenic and oxygenic phototrophs ( Philippi et al 2021 ; Watanabe and Horiike 2021 ); and anaerobic chemoorganotrophs ( Li et al 2019 ). Many of the remaining Nif bacteria are symbiotic with plants ( Li et al 2015 ; de Lajudie and Young 2017 ; Roy et al 2020 ) or animals ( Russell et al 2009 ; König et al 2016 ; Shukla et al 2016 ).…”

Section: Introductionmentioning

confidence: 99%

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Origin and Evolution of Nitrogen Fixation in Prokaryotes

Lin

Chen

et al. 2022

Molecular Biology and Evolution

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The origin of nitrogen fixation is an important issue in evolutionary biology. While nitrogen is required by all living organisms, only a small fraction of bacteria and archaea can fix nitrogen. The prevailing view is that nitrogen fixation first evolved in archaea and was later transferred to bacteria. However, nitrogen-fixing bacteria are far larger in number and far more diverse in ecological niches than nitrogen-fixing archaea. We therefore propose the bacteria-first hypothesis, which postulates that nitrogen fixation first evolved in bacteria and was later transferred to archaea. As >30,000 prokaryotic genomes have been sequenced, we conduct an in-depth comparison of the two hypotheses. We first identify the six genes involved in nitrogen fixation in all sequenced prokaryotic genomes and then reconstruct phylogenetic trees using the six nitrogen-fixing (Nif) proteins individually or in combination. In each of these trees the earliest lineages are bacterial Nif protein sequences and in the oldest clade (group) the archaeal sequences are all nested inside bacterial sequences, suggesting that the Nif proteins first evolved in bacteria. The bacteria-first hypothesis is further supported by the observation that the majority of nitrogen-fixing archaea carry the major bacterial Mo (molybdenum) transporter (ModABC) rather than the archaeal Mo transporter (WtpABC). Moreover, in our phylogeny of all available ModA and WtpA protein sequences the earliest lineages are bacterial sequences while archaeal sequences are nested inside bacterial sequences. Furthermore, the bacteria-first hypothesis is supported by available isotopic data. In conclusion, our study strongly supports the bacteria-first hypothesis.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Origin and Evolution of Nitrogen Fixation in Prokaryotes

Lin

Chen

et al. 2022

Molecular Biology and Evolution

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“…All three nitrogenase forms are structurally and functionally similar, each containing two protein components: a dinitrogenase reductase (NifH, VnfH, or AnfH) and a catalytic component (NifDK, VnfDGK, or AnfDGK). Most biological N 2 fixation is catalyzed by the more efficient Mo-Fe nitrogenase, while Fe-V and Fe-Fe nitrogenases are alternative enzymes used in Mo-limited settings 19 , 20 . A combination of rate measurements, lab cultivation, flow cytometry, molecular analysis, and cellular imaging have revealed that diazotrophs are active throughout the oceans.…”

Section: Introductionmentioning

confidence: 99%

Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments

et al. 2022

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Microbially mediated nitrogen cycling in carbon-dominated cold seep environments remains poorly understood. So far anaerobic methanotrophic archaea (ANME-2) and their sulfate-reducing bacterial partners (SEEP-SRB1 clade) have been identified as diazotrophs in deep sea cold seep sediments. However, it is unclear whether other microbial groups can perform nitrogen fixation in such ecosystems. To fill this gap, we analyzed 61 metagenomes, 1428 metagenome-assembled genomes, and six metatranscriptomes derived from 11 globally distributed cold seeps. These sediments contain phylogenetically diverse nitrogenase genes corresponding to an expanded diversity of diazotrophic lineages. Diverse catabolic pathways were predicted to provide ATP for nitrogen fixation, suggesting diazotrophy in cold seeps is not necessarily associated with sulfate-dependent anaerobic oxidation of methane. Nitrogen fixation genes among various diazotrophic groups in cold seeps were inferred to be genetically mobile and subject to purifying selection. Our findings extend the capacity for diazotrophy to five candidate phyla (Altarchaeia, Omnitrophota, FCPU426, Caldatribacteriota and UBA6262), and suggest that cold seep diazotrophs might contribute substantially to the global nitrogen balance.

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“…It has only recently been shown that even under Mo limitation alternative N 2 fixers will try to acquire enough of this trace metal to still sustain their nif nitrogenase instead of expressing the alternative nitrogenases (Philippi et al, 2021). Thus, the presence of alternative nitrogenases, while being a given, is not explainable for us right now.…”

Section: Alternative Nitrogenases and Diazotrophs Across Omz Watersmentioning

confidence: 99%

Nitrogenases in Oxygen Minimum Zone Waters

Reeder

Löscher

2022

Front. Mar. Sci.

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Biological dinitrogen (N2) fixation is the pathway making the large pool of atmospheric N2 available to marine life. Besides direct rate measurements, a common approach to explore the potential for N2 fixation in the ocean is a screening-based targeting the key functional marker gene nifH, coding for a subunit of the nitrogenase reductase. As novel sequencing techniques improved, our understanding of the diversity of marine N2 fixers grew exponentially. However, one aspect of N2 fixation in the ocean is often underexplored, which are the two alternative types of the key enzyme of N2 fixation, the nitrogenase. Altogether there are three isoenzymes, the most common Mo-Fe nitrogenase Nif, the Fe-Fe nitrogenase Anf, and the V-Fe nitrogenase Vnf, which differ regarding their genetic organization, as well as their metal co-enzymes. While Mo is only available in the presence of at least traces of oxygen (O2), V and Fe are available if O2 is absent. Therefore, low O2 and anoxic ocean environments could be an ideal place to explore the diversity of the different isotypes of the nitrogenases. Most phylogenetic studies, however, were only based on the functional marker gene nifH, encoding for a subunit of the Nif nitrogenase, and thus limited in representing the diversity of alternative nitrogenases. Here, we screened metagenomes and -transcriptomes from O2 minimum zones off Peru, from the Bay of Bengal, and the anoxic Saanich Inlet to explore the diversity of genes involved in N2 fixation. We identified genes related to all three nitrogenases, and a generally increased diversity as compared to our previous nifH based on studies from OMZ waters. While we could not confirm gene expression of alternative nitrogenases from our transcriptomic, we detected diazotrophs harboring the genetic potential for alternative nitrogenases. We suggest that alternative nitrogenases may not be used under conditions present in those waters, however, depending on trace metal availability they may become active under future ocean deoxygenation.

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Purple sulfur bacteria fix N2 via molybdenum-nitrogenase in a low molybdenum Proterozoic ocean analogue

Cited by 27 publications

References 100 publications

Origin and Evolution of Nitrogen Fixation in Prokaryotes

Origin and Evolution of Nitrogen Fixation in Prokaryotes

Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments

Nitrogenases in Oxygen Minimum Zone Waters

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