Phylogenetic analysis of NAP, an unconventional actin of the Volvocales

Kato-Minoura, Takako; Karino, Kumiko; Akimoto, Nobuyuki; Yoshiga, Norito; Ehara, Mika; Aoki, Seishiro

doi:10.1007/s00606-014-1187-5

Cited by 6 publications

(6 citation statements)

References 29 publications

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“…Indeed, one of the five amino acid residues directly involved in hydrogen bonding between rabbit-muscle actin and LatA (Morton et al 2000) is altered in NAP1 (His for Tyr at position 73: Figure 1B). This simple model would be consistent with the near-normal phenotype of the ida5-1 mutant but would seem to require exposure of the ancestors of modern Chlamydomonas (and related Volvocales algae, the only other organisms in which close homologs of NAP1 have been found: Kato-Minoura et al 2014) to a latrunculin-like toxin during evolution. Although the latrunculins themselves are the products of marine sponges (Spector et al 1983), and Chlamydomonas lives in fresh water, such an exposure is certainly possible.…”

Section: Discussionmentioning

confidence: 61%

“…Numbers, bootstrap values; scale bar, evolutionary distance in substitutions per residue. For a more in-depth phylogenetic analysis of the Chlamydomonas and other actins, see Kato-Minoura et al (2014). (B) Amino acidsequence alignment of the Chlamydomonas actins (Cr IDA5 and Cr NAP1) with human skeletal a-actin (Hs a-actin) and sites of the NAP1 LatBsensitivity and IDA5 LatB-resistance mutations identified in this study.…”

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confidence: 99%

“…However, interpretation of this surprising hypothesis has been complicated by the presence in Chlamydomonas of a gene (NAP1) that encodes an unconventional actin (Kato-Minoura et al 1998). Although NAP1 is only $65% identical in amino acid sequence to IDA5 and other conventional actins ( Figure 1B), phylogenetic analyses consistently cluster it together with actins rather than with Arp1-type actin-related proteins ( Figure 1A; Kato-Minoura et al 2014). NAP1 is transcriptionally upregulated in the ida5-1 null mutant (Kato-Minoura et al 1998;Hirono et al 2003), so that it has been speculated that it could provide actin function under these conditions.…”

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confidence: 99%

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Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

2015

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Actin is one of the most conserved eukaryotic proteins. It is thought to have multiple essential cellular roles and to function primarily or exclusively as filaments ("F-actin"). Chlamydomonas has been an enigma, because a null mutation (ida5-1) in its single gene for conventional actin does not affect growth. A highly divergent actin gene, NAP1, is upregulated in ida5-1 cells, but it has been unclear whether NAP1 can form filaments or provide actin function. Here, we used the actin-depolymerizing drug latrunculin B (LatB), the F-actin-specific probe Lifeact-Venus, and genetic and molecular methods to resolve these issues. LatB-treated wild-type cells continue to proliferate; they initially lose Lifeact-stained structures but recover them concomitant with upregulation of NAP1. Thirty-nine LatB-sensitive mutants fell into four genes (NAP1 and LAT1-LAT3) in which we identified the causative mutations using a novel combinatorial pool-sequencing strategy. LAT1-LAT3 are required for NAP1 upregulation upon LatB treatment, and ectopic expression of NAP1 largely rescues the LatB sensitivity of the lat1-lat3 mutants, suggesting that the LAT gene products comprise a regulatory hierarchy with NAP1 expression as the major functional output. Selection of LatB-resistant revertants of a nap1 mutant yielded dominant IDA5 mutations that presumably render F-IDA5 resistant to LatB, and nap1 and lat mutations are synthetically lethal with ida5-1 in the absence of LatB. We conclude that both IDA5 and the divergent NAP1 can form filaments and redundantly provide essential F-actin functions and that a novel surveillance system, probably responding to a loss of F-actin, triggers NAP1 expression and perhaps other compensatory responses.

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Section: Discussionmentioning

confidence: 61%

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confidence: 99%

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confidence: 99%

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Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

2015

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“…Chlamydomonas cleavage furrows have both actin and tubulin and dynamin-like vesicle secretion as well as intraflagellar transport (IFT) proteins suggesting they all are involved in cytokinesis (Cross and Umen 2015). A role for actin was hard to establish as volvocalean algae have two actins (Kato-Minoura et al 2015): conventional actin and a rapidly evolving actin paralogue that may function primarily in ciliary regeneration (Kato-Minoura 2005), but can substitute for standard actin in null mutants for several functions including cytokinesis (Hirono et al 2003;Kato-Minoura et al 1997;Onishi et al 2016).…”

Section: Cytokinesis Diversification In Eukaryotesmentioning

confidence: 99%

Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria)

Cavalier‐Smith

Chao

2020

Protoplasma

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Palaeontologically, eubacteria are > 3× older than neomura (eukaryotes, archaebacteria). Cell biology contrasts ancestral eubacterial murein peptidoglycan walls and derived neomuran N-linked glycoprotein coats/walls. Misinterpreting long stems connecting clade neomura to eubacteria on ribosomal sequence trees (plus misinterpreted protein paralogue trees) obscured this historical pattern. Universal multiprotein ribosomal protein (RP) trees, more accurate than rRNA trees, are taxonomically undersampled. To reduce contradictions with genically richer eukaryote trees and improve eubacterial phylogeny, we constructed site-heterogeneous and maximum-likelihood universal three-domain, two-domain, and single-domain trees for 143 eukaryotes (branching now congruent with 187-protein trees), 60 archaebacteria, and 151 taxonomically representative eubacteria, using 51 and 26 RPs. Site-heterogeneous trees greatly improve eubacterial phylogeny and higher classification, e.g. showing gracilicute monophyly, that many ‘rDNA-phyla’ belong in Proteobacteria, and reveal robust new phyla Synthermota and Aquithermota. Monoderm Posibacteria and Mollicutes (two separate wall losses) are both polyphyletic: multiple outer membrane losses in Endobacteria occurred separately from Actinobacteria; neither phylum is related to Chloroflexi, the most divergent prokaryotes, which originated photosynthesis (new model proposed). RP trees support an eozoan root for eukaryotes and are consistent with archaebacteria being their sisters and rooted between Filarchaeota (=Proteoarchaeota, including ‘Asgardia’) and Euryarchaeota sensu-lato (including ultrasimplified ‘DPANN’ whose long branches often distort trees). Two-domain trees group eukaryotes within Planctobacteria, and archaebacteria with Planctobacteria/Sphingobacteria. Integrated molecular/palaeontological evidence favours negibacterial ancestors for neomura and all life. Unique presence of key pre-neomuran characters favours Planctobacteria only as ancestral to neomura, which apparently arose by coevolutionary repercussions (explained here in detail, including RP replacement) of simultaneous outer membrane and murein loss. Planctobacterial C-1 methanotrophic enzymes are likely ancestral to archaebacterial methanogenesis and β-propeller-α-solenoid proteins to eukaryotic vesicle coats, nuclear-pore-complexes, and intraciliary transport. Planctobacterial chaperone-independent 4/5-protofilament microtubules and MamK actin-ancestors prepared for eukaryote intracellular motility, mitosis, cytokinesis, and phagocytosis. We refute numerous wrong ideas about the universal tree.

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“…Furthermore, the dN/dS ratios based on the branch model revealed that 93 orthogroups among the single-copy orthogroups were significantly different, with relatively high dN/dS ratios observed in three terrestrial Oedogoniales species. Previous studies have revealed that low dN/dS ratios (dN/dS < 1) denote a strong purifying selection [42], whereas relatively high dN/dS ratios could be interpreted as a weak purifying selection [80]. The relatively high dN/dS ratios observed in the three terrestrial Oedogoniales species suggested the occurrence of rapid evolution.…”

Section: Discussionmentioning

confidence: 87%

Phylotranscriptomic and Evolutionary Analyses of Oedogoniales (Chlorophyceae, Chlorophyta)

Xiong

Dong

et al. 2022

Diversity

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This study determined the transcriptomes of eight Oedogoniales species, including six species from Oedogonium and two species from Oedocladium to conduct phylotranscriptomic and evolutionary analyses. 155,952 gene families and 192 single-copy orthogroups were detected. Phylotranscriptomic analyses based on single-copy orthogroups were conducted using supermatrix and coalescent-based approaches. The phylotranscriptomic analysis results revealed that Oedogonium is polyphyletic, and Oedocladium clustered with Oedogonium. Together with the transcriptomes of the OCC clade in the public database, the phylogenetic relationship of the three orders (Oedogoniales, Chaetophorales, Chaetopeltidales) is discussed. The non-synonymous (dN) to synonymous substitution (dS) ratios of single-copy orthogroups of the terrestrial Oedogoniales species using a branch model of phylogenetic analysis by maximum likelihood were estimated, which showed that 92 single-copy orthogroups were putative rapidly evolving genes. Gene Ontology enrichment and Kyoto Encyclopedia of Genes and Genomes pathway analyses results revealed that some of the rapidly evolving genes were associated with photosynthesis, implying that terrestrial Oedogoniales species experienced rapid evolution to adapt to terrestrial habitats. The phylogenetic results combined with evolutionary analyses suggest that the terrestrialization process of Oedogoniales may have occured more than once.

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Phylogenetic analysis of NAP, an unconventional actin of the Volvocales

Cited by 6 publications

References 29 publications

Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria)

Phylotranscriptomic and Evolutionary Analyses of Oedogoniales (Chlorophyceae, Chlorophyta)

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