Conservation of magnetite biomineralization genes in all domains of life and implications for magnetic sensing

Animals use geomagnetic fields for navigational cues, yet the sensory mechanism underlying magnetic perception remains poorly understood. One idea is that geomagnetic fields are physically transduced by magnetite crystals contained inside specialized receptor cells, but evidence for intracellular, biogenic magnetite in eukaryotes is scant. Certain bacteria produce magnetite crystals inside intracellular compartments, representing the most ancient form of biomineralization known and having evolved prior to emergence of the crown group of eukaryotes, raising the question of whether magnetite biomineralization in eukaryotes and prokaryotes might share a common evolutionary history. Here, we discover that salmonid olfactory epithelium contains magnetite crystals arranged in compact clusters and determine that genes differentially expressed in magnetic olfactory cells, contrasted to nonmagnetic olfactory cells, share ancestry with an ancient prokaryote magnetite biomineralization system, consistent with exaptation for use in eukaryotic magnetoreception. We also show that 11 prokaryote biomineralization genes are universally present among a diverse set of eukaryote taxa and that nine of those genes are present within the Asgard clade of archaea Lokiarchaeota that affiliates with eukaryotes in phylogenomic analysis. Consistent with deep homology, we present an evolutionary genetics hypothesis for magnetite formation among eukaryotes to motivate convergent approaches for examining magnetite-based magnetoreception, molecular origins of matrix-associated biomineralization processes, and eukaryogenesis.

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The fossil record of early eukaryotic diversification

The Paleontological Society Papers ◽

10.1017/s1089332600002321 ◽

2004 ◽

Vol 10 ◽

pp. 35-50 ◽

Cited By ~ 43

Author(s):

Susannah M. Porter

Keyword(s):

Fossil Record ◽

Main Phase ◽

Cambrian Explosion ◽

Evolution Of Sex ◽

Crown Group ◽

Long Period ◽

Stem Group ◽

Group Evolution ◽

Domains Of Life ◽

Ecology And Environment

The Cambrian explosion can be thought of as the culmination of a diversification of eukaryotes that had begun several hundred million years before. Eukaryotes - one of the three domains of life — originated by late Archean time, and probably underwent a long period of stem group evolution during the Paleoproterozoic Era. A suite of taxonomically resolved body fossils and biomarkers, together with estimates of acritarch and compression fossil diversity, suggest that while divergences among major eukaryotic clades or 'super-groups' may have occurred as early as latest Paleoproterozoic through Mesoproterozoic time, the main phase of eukaryotic diversification took place several hundred million years later, during the middle Neoproterozoic Era. Hypotheses for Neoproterozoic diversification must therefore explain why eukaryotic diversification is delayed several hundred million years after the origin of the eukaryotic crown group, and why diversification appears to have occurred independently within several eukaryotic super-groups at the same time. Evolutionary explanations for eukaryotic diversification (the evolution of sex; the acquisition of plastids) fail to account for these patterns, but ecological explanations (the advent of microbial predators) and environmental explanations (changes in ocean chemistry) are both consistent with them. Both ecology and environment may have played a role in triggering or at least fueling Neoproterozoic eukaryotic diversification.

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The evolution of YidC/Oxa/Alb3 family in the three domains of life: a phylogenomic analysis

BMC Evolutionary Biology ◽

10.1186/1471-2148-9-137 ◽

2009 ◽

Vol 9 (1) ◽

pp. 137 ◽

Cited By ~ 30

Author(s):

Yu-Juan Zhang ◽

Hai-Feng Tian ◽

Jian-Fan Wen

Keyword(s):

Phylogenomic Analysis ◽

Domains Of Life

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CTP synthase forms cytoophidia in archaea

10.1101/830091 ◽

2019 ◽

Author(s):

Shuang Zhou ◽

Hua Xiang ◽

Ji-Long Liu

Keyword(s):

De Novo ◽

Stimulated Emission ◽

Metabolic Enzyme ◽

De Novo Synthesis ◽

Low Salt ◽

Ctp Synthase ◽

Intracellular Compartments ◽

Domains Of Life ◽

Haloarcula Hispanica ◽

Rate Limiting

AbstractCTP synthase (CTPS) is an important metabolic enzyme that catalyzes the rate-limiting reaction of de novo synthesis of the nucleotide CTP. Since 2010, a series of studies have demonstrated that CTPS can form filamentous structures termed cytoophidia in bacteria and eukaryotes. However, it remains unknown whether cytoophidia exist in archaea, the third domain of life. Using Haloarcula hispanica as a model system, here we demonstrate that CTPS forms distinct intracellular compartments in archaeal cells. Under stimulated emission depletion (STED) microscopy, we find that some HhCTPS compartments have elongated filamentous structures, resembling cytoophidia in bacteria and eukaryotes. When Haloarcula cells are cultured in low-salt medium, the occurrence of cytoophidia increases dramatically. Moreover, overexpression of CTPS or glutamine analog treatment promotes cytoophidium assembly in H. hispanica. Our study reveals that CTPS forms cytoophidia in all three domains of life, suggesting that this is an ancient property of CTPS.

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Novel domain architectures and functional determinants in atypical annexins revealed by phylogenomic analysis

Biological Chemistry ◽

10.1515/hsz-2016-0273 ◽

2017 ◽

Vol 398 (7) ◽

pp. 751-763 ◽

Cited By ~ 2

Author(s):

Maria-Pilar Fernandez ◽

Montserrat Garcia ◽

Silvia Martin-Almedina ◽

Reginald O. Morgan

Keyword(s):

Molecular Interactions ◽

Calcium Binding ◽

Markov Models ◽

Functional Divergence ◽

Structural Features ◽

Phylogenomic Analysis ◽

Evolutionary Constraint ◽

Molecular Systematic ◽

Domains Of Life ◽

Canonical Type

AbstractThe fundamental cellular role and molecular interactions of annexins in vesicle trafficking and membrane remodeling remain to be further clarified in order to better understand and exploit their contributions to health and disease. We focused on distinctive features of atypical annexins from all domains of life using phylogenomic, molecular systematic and experimental approaches, to extend the current paradigm and better account for annexin diversity of structure, function and mechanistic role in membrane homeostasis. The analysis of gene duplications, organization of domain architectures and profile hidden Markov models of subfamily orthologs defined conserved structural features relevant to molecular interactions and functional divergence of seven family clades ANXA-G. Single domain annexins of bacteria, including cyanobacteria, were frequently coupled to enzymatic units conceivably related to membrane metabolism and remodeling. Multiple ANX domains (up to 20) and various distinct functional domains were observed in unique annexins. Canonical type 2 calcium binding ligands were well-preserved in roughly half of all ANX domains, but alternative structural motifs comprised of ‘KGD’, cysteine or tryptophan residues were prominently conserved in the same strategic interhelical loops. Selective evolutionary constraint, site-specific location and co-occurrence in all kingdoms identify alternative modes of fundamental binding interactions for annexins.

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Evolution of intracellular compartmentalization

Biochemical Journal ◽

10.1042/bj20120957 ◽

2012 ◽

Vol 449 (2) ◽

pp. 319-331 ◽

Cited By ~ 80

Author(s):

Yoan Diekmann ◽

José B. Pereira-Leal

Keyword(s):

Genetic Basis ◽

Present Review ◽

Evolutionary Processes ◽

Tissue Specific ◽

Evolutionary Origins ◽

Intracellular Compartments ◽

Domains Of Life ◽

Physical Barriers ◽

Cell Plan ◽

Intracellular Compartmentalization

Cells compartmentalize their biochemical functions in a variety of ways, notably by creating physical barriers that separate a compartment via membranes or proteins. Eukaryotes have a wide diversity of membrane-based compartments, many that are lineage- or tissue-specific. In recent years, it has become increasingly evident that membrane-based compartmentalization of the cytosolic space is observed in multiple prokaryotic lineages, giving rise to several types of distinct prokaryotic organelles. Endosymbionts, previously believed to be a hallmark of eukaryotes, have been described in several bacteria. Protein-based compartments, frequent in bacteria, are also found in eukaryotes. In the present review, we focus on selected intracellular compartments from each of these three categories, membrane-based, endosymbiotic and protein-based, in both prokaryotes and eukaryotes. We review their diversity and the current theories and controversies regarding the evolutionary origins. Furthermore, we discuss the evolutionary processes acting on the genetic basis of intracellular compartments and how those differ across the domains of life. We conclude that the distinction between eukaryotes and prokaryotes no longer lies in the existence of a compartmentalized cell plan, but rather in its complexity.

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