New Alphaproteobacteria Thrive in the Depths of the Ocean with Oxygen Gradient

Abstract

We survey here the Alphaproteobacteria, a large class encompassing physiologically diverse bacteria which are divided in several orders established since 2007. Currently, there is considerable uncertainty regarding the classification of an increasing number of marine metagenome-assembled genomes (MAGs) that remain poorly defined in their taxonomic position within Alphaproteobacteria. The traditional classification of NCBI taxonomy is increasingly complemented by the Genome Taxonomy Database (GTDB), but the two taxonomies differ considerably in the classification of several Alphaproteobacteria, especially from ocean metagenomes. We analyzed the classification of Alphaproteobacteria lineages that are most common in marine environments, using integrated approaches of phylogenomics and functional profiling of metabolic features that define their aerobic metabolism. Using protein markers such as NuoL, the largest membrane subunit of complex I, we have identified new clades of Alphaproteobacteria that are specific to marine niches with steep oxygen gradients (oxycline). These bacteria have relatives among MAGs found in anoxic strata of Lake Tanganyika and together define a lineage that is distinct from either Rhodospirillales or Sneathiellales. We characterized in particular the new ‘oxycline’ clade. Our analysis of Alphaproteobacteria also reveals new clues regarding the ancestry of mitochondria, which likely evolved in oxycline marine environments.

On the bacterial ancestry of mitochondria: new insights with triangulated approaches

“…Iterative PSI-BLAST searches of representative proteins [2,43] were carried out to evaluate their completeness and re-annotation congruity.…”

“…We routinely kept the recently identified New clades of marine MAGs as a separate lineage from related Sneathiellales (including also Minwuiales) because of the diversity in their bioenergetic traits [2]. We also kept the lineage of Iodidimonadales separate from other SERIK groups [2] essentially because of their unique synteny of M16B-ISP (Fig. 1 and Supplementary Fig.…”

“…The latter was considered for its common presence in alphaproteobacteria with reduced genomes including Rickettiales and early branching eukaryotes (Supplementary Table S2). We also evaluated the distribution of genes for M16A peptidases, which have multiple homologs in eukaryotes [26] (Box1; see Methods for more detail), but have not been considered before in relation to eukaryogenesis [1][2][3][4][5][6][7][8]13]. Figure 2 presents the lineage-specific distribution of the selected aerobic traits in quantitative terms, showing an apparent peak around Iodidimonadales.…”

“…S3A). The cumulative distribution of OFORs genes is uneven along the various lineages, with maximal concentration in marine New clades [2] (Fig. 5 and Supplementary Fig.…”

“…Previous research has primarily relied on phylogenetic inference to identify the possible bacterial relatives and ancestors of mitochondria, hereafter called protomitochondria. However, this approach has produced inconsistent and varying results depending on the phylogenetic approach, taxonomic sampling, and corrections used to reduce artefacts [1][2][3][4][5][6][7][8]. In fact, almost all major lineages of alphaproteobacteria have been proposed as protomitochondria relatives.…”