Comparative Genomics on Cultivated and Uncultivated Freshwater and Marine “CandidatusManganitrophaceae” Species Implies Their Worldwide Reach in Manganese Chemolithoautotrophy
Abstract:Manganese (Mn) is an abundant redox-active metal that cycles in many of Earth’s biomes. While diverse bacteria and archaea have been demonstrated to respire Mn(III/IV), only recently have bacteria been implicated in Mn(II) oxidation-dependent growth.
“…Manganitrophaceae ), which have been analyzed in detail recently (Fig. 8 , Supplementary Figure 10 ) [ 77 , 78 ]. Fig.…”
Section: Resultsmentioning
confidence: 99%
“…6 ). Next is the Nitrospirota order SBBL01 , containing recently described manganese-oxidizers [ 77 , 78 ]. Genomes in this clade contain unique cytochromes involved in manganese oxidation that have been discussed in detail (Fig.…”
Section: Discussionmentioning
confidence: 99%
“…Genomes in this clade contain unique cytochromes involved in manganese oxidation that have been discussed in detail (Fig. 8 , Supplementary Figure 10 ) [ 78 ].…”
The phyla Nitrospirota and Nitrospinota have received significant research attention due to their unique nitrogen metabolisms important to biogeochemical and industrial processes. These phyla are common inhabitants of marine and terrestrial subsurface environments and contain members capable of diverse physiologies in addition to nitrite oxidation and complete ammonia oxidation. Here, we use phylogenomics and gene-based analysis with ancestral state reconstruction and gene-tree–species-tree reconciliation methods to investigate the life histories of these two phyla. We find that basal clades of both phyla primarily inhabit marine and terrestrial subsurface environments. The genomes of basal clades in both phyla appear smaller and more densely coded than the later-branching clades. The extant basal clades of both phyla share many traits inferred to be present in their respective common ancestors, including hydrogen, one-carbon, and sulfur-based metabolisms. Later-branching groups, namely the more frequently studied classes Nitrospiria and Nitrospinia, are both characterized by genome expansions driven by either de novo origination or laterally transferred genes that encode functions expanding their metabolic repertoire. These expansions include gene clusters that perform the unique nitrogen metabolisms that both phyla are most well known for. Our analyses support replicated evolutionary histories of these two bacterial phyla, with modern subsurface environments representing a genomic repository for the coding potential of ancestral metabolic traits.
“…Manganitrophaceae ), which have been analyzed in detail recently (Fig. 8 , Supplementary Figure 10 ) [ 77 , 78 ]. Fig.…”
Section: Resultsmentioning
confidence: 99%
“…6 ). Next is the Nitrospirota order SBBL01 , containing recently described manganese-oxidizers [ 77 , 78 ]. Genomes in this clade contain unique cytochromes involved in manganese oxidation that have been discussed in detail (Fig.…”
Section: Discussionmentioning
confidence: 99%
“…Genomes in this clade contain unique cytochromes involved in manganese oxidation that have been discussed in detail (Fig. 8 , Supplementary Figure 10 ) [ 78 ].…”
The phyla Nitrospirota and Nitrospinota have received significant research attention due to their unique nitrogen metabolisms important to biogeochemical and industrial processes. These phyla are common inhabitants of marine and terrestrial subsurface environments and contain members capable of diverse physiologies in addition to nitrite oxidation and complete ammonia oxidation. Here, we use phylogenomics and gene-based analysis with ancestral state reconstruction and gene-tree–species-tree reconciliation methods to investigate the life histories of these two phyla. We find that basal clades of both phyla primarily inhabit marine and terrestrial subsurface environments. The genomes of basal clades in both phyla appear smaller and more densely coded than the later-branching clades. The extant basal clades of both phyla share many traits inferred to be present in their respective common ancestors, including hydrogen, one-carbon, and sulfur-based metabolisms. Later-branching groups, namely the more frequently studied classes Nitrospiria and Nitrospinia, are both characterized by genome expansions driven by either de novo origination or laterally transferred genes that encode functions expanding their metabolic repertoire. These expansions include gene clusters that perform the unique nitrogen metabolisms that both phyla are most well known for. Our analyses support replicated evolutionary histories of these two bacterial phyla, with modern subsurface environments representing a genomic repository for the coding potential of ancestral metabolic traits.
“…Despite their widespread distribution and the important roles of Nitrospirota in biogeochemical cycles of iron, manganese, and nitrogen (37)(38)(39)(40)(41), many aspects of their chemotaxonomy and bioenergetics remain understudied. Genome-based bioenergetic models implicate the presence of ETCs in aerobic and anaerobic Nitrospirota (41)(42)(43)(44)(45), yet their corresponding respiratory quinones have not been studied.…”
Section: Novel Respiratory Quinones In Nitrospirotamentioning
The dominant organisms in modern oxic ecosystems rely on respiratory quinones with high redox potential (HPQs) for electron transport in aerobic respiration and photosynthesis. The diversification of quinones, from low redox potential in anaerobes to HPQs in aerobes, is assumed to have followed Earth's surface oxygenation ~2.3 billion years ago. However, the evolutionary origins of HPQs remain unresolved. Here, we reconstruct the biosynthetic pathway of a novel HPQ, methyl-plastoquinone, that is unique to bacteria of the phylum Nitrospirota. We demonstrate that the three extant HPQ biosynthetic pathways, in Nitrospirota, Cyanobacteriota, and Pseudomonadota, share a common origin that predates the emergence of these phyla. We show that aerobic metabolism using HPQs is ancestral to Cyanobacteriota and Pseudomonadota and significantly predates Earth's surface oxygenation.
“…However, these taxa were clearly conceived as not containing the genus Nitrospira although they did cover Thermodesulfovibrio , among other genera. Recent studies did not indicate a close relationship between Nitrospira and Leptospirillum either [42]. For this reason, the best option to fill the gaps appears to be to propose names at the rank of class, order and family that only harbour the genus Nitrospira , and to attribute them to the original authors [35].…”
Section: Names That Are Not Validly Publishedmentioning
The International Code of Nomenclature of Prokaryotes (ICNP) recently underwent some major modifications regarding the higher taxonomic ranks. On the one hand, the phylum category was introduced into the ICNP, which rapidly led to the valid publication of more than forty names of phyla. On the other hand, a decision on the retroactivity of Rule 8 regarding the names of classes was made, which removed most of the nomenclatural uncertainty that had affected those names during the last decade. However, it turned out that a number of names at the ranks of class, order and family are either not validly published or are validly published but illegitimate, although these names occur in the literature and are based on the type genus of a phylum with a validly published name. A closer examination of the literature for these and similar cases indicates that the names are unavailable under the ICNP either because of minor formal errors in the original descriptions, because another name should have been adopted for the taxon when the name was proposed, because of taxonomic uncertainties that were settled in the meantime, or because the names were placed on the list of rejected names. The purpose of this article is to fill the gaps by providing the missing formal descriptions and to ensure that the resulting taxon names are attributed to the original authors who did the taxonomic work.
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