Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis

Abstract

Background: The Archaea are highly diverse in terms of their physiology, metabolism and ecology. Presently, very few molecular characteristics are known that are uniquely shared by either all archaea or the different main groups within archaea. The evolutionary relationships among different groups within the Euryarchaeota branch are also not clearly understood.

Results: We have carried out comprehensive analyses on each open reading frame (ORFs) in the genomes of 11 archaea (3 Crenarchaeota--Aeropyrum pernix, Pyrobaculum aerophilum and Sulfolobus acidocaldarius; 8 Euryarchaeota--Pyrococcus abyssi, Methanococcus maripaludis, Methanopyrus kandleri, Methanococcoides burtonii, Halobacterium sp. NCR-1, Haloquadratum walsbyi, Thermoplasma acidophilum and Picrophilus torridus) to search for proteins that are unique to either all Archaea or for its main subgroups. These studies have identified 1448 proteins or ORFs that are distinctive characteristics of Archaea and its various subgroups and whose homologues are not found in other organisms. Six of these proteins are unique to all Archaea, 10 others are only missing in Nanoarchaeum equitans and a large number of other proteins are specific for various main groups within the Archaea (e.g. Crenarchaeota, Euryarchaeota, Sulfolobales and Desulfurococcales, Halobacteriales, Thermococci, Thermoplasmata, all methanogenic archaea or particular groups of methanogens). Of particular importance is the observation that 31 proteins are uniquely present in virtually all methanogens (including M. kandleri) and 10 additional proteins are only found in different methanogens as well as A. fulgidus. In contrast, no protein was exclusively shared by various methanogen and any of the Halobacteriales or Thermoplasmatales. These results strongly indicate that all methanogenic archaea form a monophyletic group exclusive of other archaea and that this lineage likely evolved from Archaeoglobus. In addition, 15 proteins that are uniquely shared by M. kandleri and Methanobacteriales suggest a close evolutionary relationship between them. In contrast to the phylogenomics studies, a monophyletic grouping of archaea is not supported by phylogenetic analyses based on protein sequences.

Conclusion: The identified archaea-specific proteins provide novel molecular markers or signature proteins that are distinctive characteristics of Archaea and all of its major subgroups. The species distributions of these proteins provide novel insights into the evolutionary relationships among different groups within Archaea, particularly regarding the origin of methanogenesis. Most of these proteins are of unknown function and further studies should lead to discovery of novel biochemical and physiological characteristics that are unique to either all archaea or its different subgroups.

Figure 1

A neighbour-joining distance tree based on a concatenated sequence alignment for 31 widely distributed proteins. The numbers on the nodes indicate bootstrap scores observed in NJ/ML/MP analyses. The species shaded in yellow were selected as the query genomes for blast searches.

Figure 2

Interpretive diagrams showing the suggested evolutionary stages where genes for some of the signature proteins that are specific for the Crenarchaeota and Euryarchaeota as well as some of the Crenarchaeota subgroups, likely originated. The top diagram (A) indicates the evolutionary interpretation of the signature proteins in the absence of any other information, whereas that below (B) indicates our interpretation of this data taking into consideration other relevant information discussed in the text. The branching pattern shown here is unrooted and the proteins that are shared by all archaea were introduced in a common ancestor of all archaea. The dotted line for N. equitans in (B) indicates that its placement within Euryarchaeota lineage is uncertain. The abbreviations T and AF in these figures as well as others refer to tables and Additional files.

Figure 3

An interpretive diagram showing the evolutionary stages where genes for different proteins that are specific for methanogenic archaea likely originated. The 10 proteins that are uniquely shared by A. fulgidus and various methanogenic archaea indicate that this lineage is the closest ancestor of all methanogens.

Figure 4

A summary diagram showing the branching order of different groups within archaea based upon species distribution patterns of various archaeal-specific proteins. The arrows mark the suggested evolutionary stages where proteins that are uniquely shared by the indicated groups were introduced. The details of these proteins can be found in the indicated tables (T) or Additional files (AF). The branching pattern shown here is unrooted. The dotted line for N. equitans indicates that its placement within Euryarchaeota is uncertain. The dotted line extending from the proteins found in all archaea indicates that one cannot use this to root the archaeal tree.