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1.
Cell ; 158(1): 213-25, 2014 Jul 03.
Article in English | MEDLINE | ID: mdl-24995987

ABSTRACT

The availability of diverse genomes makes it possible to predict gene function based on shared evolutionary history. This approach can be challenging, however, for pathways whose components do not exhibit a shared history but rather consist of distinct "evolutionary modules." We introduce a computational algorithm, clustering by inferred models of evolution (CLIME), which inputs a eukaryotic species tree, homology matrix, and pathway (gene set) of interest. CLIME partitions the gene set into disjoint evolutionary modules, simultaneously learning the number of modules and a tree-based evolutionary history that defines each module. CLIME then expands each module by scanning the genome for new components that likely arose under the inferred evolutionary model. Application of CLIME to ∼1,000 annotated human pathways and to the proteomes of yeast, red algae, and malaria reveals unanticipated evolutionary modularity and coevolving components. CLIME is freely available and should become increasingly powerful with the growing wealth of eukaryotic genomes.


Subject(s)
Algorithms , Cluster Analysis , Phylogeny , Humans , Mitochondria/metabolism , Plasmodium falciparum/genetics , Plasmodium falciparum/metabolism , Proteome/analysis , Rhodophyta/genetics , Rhodophyta/metabolism , Signal Transduction , Yeasts/genetics , Yeasts/metabolism
2.
Proc Natl Acad Sci U S A ; 121(11): e2319658121, 2024 Mar 12.
Article in English | MEDLINE | ID: mdl-38442179

ABSTRACT

Light-harvesting complexes (LHCs) are diversified among photosynthetic organisms, and the structure of the photosystem I-LHC (PSI-LHCI) supercomplex has been shown to be variable depending on the species of organisms. However, the structural and evolutionary correlations of red-lineage LHCs are unknown. Here, we determined a 1.92-Å resolution cryoelectron microscopic structure of a PSI-LHCI supercomplex isolated from the red alga Cyanidium caldarium RK-1 (NIES-2137), which is an important taxon in the Cyanidiophyceae. We subsequently investigated the correlations of PSI-LHCIs from different organisms through structural comparisons and phylogenetic analysis. The PSI-LHCI structure obtained shows five LHCI subunits surrounding a PSI-monomer core. The five LHCIs are composed of two Lhcr1s, two Lhcr2s, and one Lhcr3. Phylogenetic analysis of LHCs bound to PSI in the red-lineage algae showed clear orthology of LHCs between C. caldarium and Cyanidioschyzon merolae, whereas no orthologous relationships were found between C. caldarium Lhcr1-3 and LHCs in other red-lineage PSI-LHCI structures. These findings provide evolutionary insights into conservation and diversity of red-lineage LHCs associated with PSI.


Subject(s)
Photosystem I Protein Complex , Rhodophyta , Phylogeny , Photosystem I Protein Complex/genetics , Biological Evolution , Cryoelectron Microscopy , Rhodophyta/genetics
3.
J Cell Sci ; 137(14)2024 Jul 15.
Article in English | MEDLINE | ID: mdl-38940185

ABSTRACT

Mitochondrial biogenesis relies on hundreds of proteins that are derived from genes encoded in the nucleus. According to the characteristic properties of N-terminal targeting peptides (TPs) and multi-step authentication by the protein translocase called the TOM complex, nascent polypeptides satisfying the requirements are imported into mitochondria. However, it is unknown whether eukaryotic cells with a single mitochondrion per cell have a similar complexity of presequence requirements for mitochondrial protein import compared to other eukaryotes with multiple mitochondria. Based on putative mitochondrial TP sequences in the unicellular red alga Cyanidioschyzon merolae, we designed synthetic TPs and showed that functional TPs must have at least one basic residue and a specific amino acid composition, although their physicochemical properties are not strictly determined. Combined with the simple composition of the TOM complex in C. merolae, our results suggest that a regional positive charge in TPs is verified solely by TOM22 for mitochondrial protein import in C. merolae. The simple authentication mechanism indicates that the monomitochondrial C. merolae does not need to increase the cryptographic complexity of the lock-and-key mechanism for mitochondrial protein import.


Subject(s)
Mitochondria , Mitochondrial Proteins , Protein Transport , Rhodophyta , Rhodophyta/metabolism , Rhodophyta/genetics , Mitochondrial Proteins/metabolism , Mitochondrial Proteins/genetics , Mitochondria/metabolism , Amino Acid Sequence
4.
Nature ; 579(7797): 146-151, 2020 03.
Article in English | MEDLINE | ID: mdl-32076272

ABSTRACT

Photosynthetic organisms have developed various light-harvesting systems to adapt to their environments1. Phycobilisomes are large light-harvesting protein complexes found in cyanobacteria and red algae2-4, although how the energies of the chromophores within these complexes are modulated by their environment is unclear. Here we report the cryo-electron microscopy structure of a 14.7-megadalton phycobilisome with a hemiellipsoidal shape from the red alga Porphyridium purpureum. Within this complex we determine the structures of 706 protein subunits, including 528 phycoerythrin, 72 phycocyanin, 46 allophycocyanin and 60 linker proteins. In addition, 1,598 chromophores are resolved comprising 1,430 phycoerythrobilin, 48 phycourobilin and 120 phycocyanobilin molecules. The markedly improved resolution of our structure compared with that of the phycobilisome of Griffithsia pacifica5 enabled us to build an accurate atomic model of the P. purpureum phycobilisome system. The model reveals how the linker proteins affect the microenvironment of the chromophores, and suggests that interactions of the aromatic amino acids of the linker proteins with the chromophores may be a key factor in fine-tuning the energy states of the chromophores to ensure the efficient unidirectional transfer of energy.


Subject(s)
Cryoelectron Microscopy , Energy Transfer , Phycobilisomes/chemistry , Phycobilisomes/ultrastructure , Porphyridium/chemistry , Porphyridium/ultrastructure , Algal Proteins/chemistry , Algal Proteins/metabolism , Algal Proteins/ultrastructure , Models, Molecular , Photosynthesis , Phycobilins/chemistry , Phycobilins/metabolism , Phycobilisomes/metabolism , Protein Conformation , Protein Subunits/chemistry , Protein Subunits/metabolism , Rhodophyta/chemistry , Rhodophyta/ultrastructure
5.
Semin Cell Dev Biol ; 134: 4-13, 2023 01 30.
Article in English | MEDLINE | ID: mdl-35339358

ABSTRACT

Extremophiles have always garnered great interest because of their exotic lifestyles and ability to thrive at the physical limits of life. In hot springs environments, the Cyanidiophyceae red algae are the only photosynthetic eukaryotes able to live under extremely low pH (0-5) and relatively high temperature (35ºC to 63ºC). These extremophiles live as biofilms in the springs, inhabit acid soils near the hot springs, and form endolithic populations in the surrounding rocks. Cyanidiophyceae represent a remarkable source of knowledge about the evolution of extremophilic lifestyles and their genomes encode specialized enzymes that have applied uses. Here we review the evolutionary origin, taxonomy, genome biology, industrial applications, and use of Cyanidiophyceae as genetic models. Currently, Cyanidiophyceae comprise a single order (Cyanidiales), three families, four genera, and nine species, including the well-known Cyanidioschyzon merolae and Galdieria sulphuraria. These algae have small, gene-rich genomes that are analogous to those of prokaryotes they live and compete with. There are few spliceosomal introns and evidence exists for horizontal gene transfer as a driver of local adaptation to gain access to external fixed carbon and to extrude toxic metals. Cyanidiophyceae offer a variety of commercial opportunities such as phytoremediation to detoxify contaminated soils or waters and exploitation of their mixotrophic lifestyles to support the efficient production of bioproducts such as phycocyanin and floridosides. In terms of exobiology, Cyanidiophyceae are an ideal model system for understanding the evolutionary effects of foreign gene acquisition and the interactions between different organisms inhabiting the same harsh environment on the early Earth. Finally, we describe ongoing research with C. merolae genetics and summarize the unique insights they offer to the understanding of algal biology and evolution.


Subject(s)
Extremophiles , Rhodophyta , Humans , Eukaryota , Extremophiles/genetics , Rhodophyta/genetics , Genome , Soil , Phylogeny
6.
Semin Cell Dev Biol ; 134: 14-26, 2023 01 30.
Article in English | MEDLINE | ID: mdl-35428563

ABSTRACT

Red algae of the order Bangiales are notable for exhibiting flexible promotion of sexual and asexual reproductive processes by environmental stresses. This flexibility indicates that a trade-off between vegetative growth and reproduction occurs in response to environmental stresses that influence the timing of phase transition within the life cycle. Despite their high phylogenetic divergence, both filamentous and foliose red alga in the order Bangiales exhibit a haploid-diploid life cycle, with a haploid leafy or filamentous gametophyte (thallus) and a diploid filamentous sporophyte (conchocelis). Unlike haploid-diploid life cycles in other orders, the gametophyte in Bangiales is generated independently of meiosis; the regulation of this generation transition is not fully understood. Based on transcriptome and gene expression analyses, the originally proposed biphasic model for alternation of generations in Bangiales was recently updated to include a third stage. Along with the haploid gametophyte and diploid sporophyte, the triphasic framework recognizes a diploid conchosporophyte-a conchosporangium generated on the conchocelis-phase and previously considered to be part of the sporophyte. In addition to this sexual life cycle, some Bangiales species have an asexual life cycle in which vegetative cells of the thallus develop into haploid asexual spores, which are then released from the thallus to produce clonal thalli. Here, we summarize the current knowledge of the triphasic life cycle and life cycle trade-off in Neopyropia yezoensis and 'Bangia' sp. as model organisms for the Bangiales.


Subject(s)
Rhodophyta , Animals , Phylogeny , Rhodophyta/genetics , Life Cycle Stages/genetics , Germ Cells, Plant , Reproduction/genetics
7.
Mol Biol Evol ; 41(2)2024 Feb 01.
Article in English | MEDLINE | ID: mdl-38267085

ABSTRACT

Cellular and physiological cycles are driven by endogenous pacemakers, the diurnal and circadian rhythms. Key functions such as cell cycle progression and cellular metabolism are under rhythmic regulation, thereby maintaining physiological homeostasis. The photoreceptors phytochrome and cryptochrome, in response to light cues, are central input pathways for physiological cycles in most photosynthetic organisms. However, among Archaeplastida, red algae are the only taxa that lack phytochromes. Current knowledge about oscillatory rhythms is primarily derived from model species such as Arabidopsis thaliana and Chlamydomonas reinhardtii in the Viridiplantae, whereas little is known about these processes in other clades of the Archaeplastida, such as the red algae (Rhodophyta). We used genome-wide expression profiling of the red seaweed Gracilariopsis chorda and identified 3,098 rhythmic genes. Here, we characterized possible cryptochrome-based regulation and photosynthetic/cytosolic carbon metabolism in this species. We found a large family of cryptochrome genes in G. chorda that display rhythmic expression over the diurnal cycle and may compensate for the lack of phytochromes in this species. The input pathway gates regulatory networks of carbon metabolism which results in a compact and efficient energy metabolism during daylight hours. The system in G. chorda is distinct from energy metabolism in most plants, which activates in the dark. The green lineage, in particular, land plants, balance water loss and CO2 capture in terrestrial environments. In contrast, red seaweeds maintain a reduced set of photoreceptors and a compact cytosolic carbon metabolism to thrive in the harsh abiotic conditions typical of intertidal zones.


Subject(s)
Arabidopsis , Rhodophyta , Seaweed , Seaweed/genetics , Cryptochromes/metabolism , Rhodophyta/genetics , Circadian Rhythm/genetics , Arabidopsis/genetics
8.
Nature ; 572(7768): 240-243, 2019 08.
Article in English | MEDLINE | ID: mdl-31316212

ABSTRACT

Rhodophyta (red algae) is one of three lineages of Archaeplastida1, a supergroup that is united by the primary endosymbiotic origin of plastids in eukaryotes2,3. Red algae are a diverse and species-rich group, members of which are typically photoautotrophic, but are united by a number of highly derived characteristics: they have relatively small intron-poor genomes, reduced metabolism and lack cytoskeletal structures that are associated with motility, flagella and centrioles. This suggests that marked gene loss occurred around their origin4; however, this is difficult to reconstruct because they differ so much from the other archaeplastid lineages, and the relationships between these lineages are unclear. Here we describe the novel eukaryotic phylum Rhodelphidia and, using phylogenomics, demonstrate that it is a closely related sister to red algae. However, the characteristics of the two Rhodelphis species described here are nearly opposite to those that define red algae: they are non-photosynthetic, flagellate predators with gene-rich genomes, along with a relic genome-lacking primary plastid that probably participates in haem synthesis. Overall, these findings alter our views of the origins of Rhodophyta, and Archaeplastida evolution as a whole, as they indicate that mixotrophic feeding-that is, a combination of predation and phototrophy-persisted well into the evolution of the group.


Subject(s)
Phylogeny , Rhodophyta/classification , Rhodophyta/metabolism , Cell Shape , Cell Survival , Genome , Photosynthesis , Rhodophyta/cytology , Rhodophyta/genetics
9.
Proc Natl Acad Sci U S A ; 119(41): e2210665119, 2022 10 11.
Article in English | MEDLINE | ID: mdl-36194630

ABSTRACT

Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria, which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically, or heterotrophically, and is being developed as an industrial source of vitamins and pigments because of its high biomass productivity. Here, we show that Galdieria exhibits a sexual life cycle, alternating between cell-walled diploid and cell wall-less haploid, and that both phases can proliferate asexually. The haploid can move over surfaces and undergo self-diploidization or generate heterozygous diploids through mating. Further, we prepared the whole genome and a comparative transcriptome dataset between the diploid and haploid and developed genetic tools for the stable gene expression, gene disruption, and selectable marker recycling system using the cell wall-less haploid. The BELL/KNOX and MADS-box transcription factors, which function in haploid-to-diploid transition and development in plants, are specifically expressed in the haploid and diploid, respectively, and are involved in the haploid-to-diploid transition in Galdieria, providing information on the missing link of the sexual life cycle evolution in Archaeplastida. Four actin genes are differently involved in motility of the haploid and cytokinesis in the diploid, both of which are myosin independent and likely reflect ancestral roles of actin. We have also generated photosynthesis-deficient mutants, such as blue-colored cells, which were depleted in chlorophyll and carotenoids, for industrial pigment production. These features of Galdieria facilitate the understanding of the evolution of algae and plants and the industrial use of microalgae.


Subject(s)
Actins , Rhodophyta , Actins/genetics , Animals , Carotenoids , Chlorophyll , Diploidy , Genomics , Haploidy , Life Cycle Stages , Plants/genetics , Rhodophyta/genetics , Transcription Factors/genetics , Vitamins
10.
Proc Natl Acad Sci U S A ; 119(34): e2208277119, 2022 08 23.
Article in English | MEDLINE | ID: mdl-35969755

ABSTRACT

Chloroplast protein import is mediated by translocons named TOC and TIC on the outer and inner envelope membranes, respectively. Translocon constituents are conserved among green lineages, including plants and green algae. However, it remains unclear whether Rhodophyta (red algae) share common chloroplast protein import mechanisms with the green lineages. We show that in the rhodophyte Cyanidioschyzon merolae, plastome-encoded Tic20pt localized to the chloroplast envelope and was transiently associated with preproteins during import, suggesting its conserved function as a TIC constituent. Besides plastome-encoded FtsHpt and several chaperones, a class of GTP (guanosine 5'-triphosphate)-binding proteins distinct from the Toc34/159 GTPase family associated transiently with preproteins. This class of proteins resides mainly in the cytosol and shows sequence similarities with Sey1/RHD3, required for endoplasmic reticulum membrane fusion, and with the periplastid-localized import factor PPP1, previously identified in the Apicomplexa and diatoms. These GTP-binding proteins, named plastid targeting factor for protein import 1 (PTF1) to PTF3, may act as plastid targeting factors in Rhodophyta.


Subject(s)
Chloroplast Proteins , GTP-Binding Proteins , Rhodophyta , Chloroplast Proteins/metabolism , Chloroplasts/metabolism , GTP-Binding Proteins/metabolism , Protein Transport , Rhodophyta/metabolism
11.
Proc Natl Acad Sci U S A ; 119(6)2022 02 08.
Article in English | MEDLINE | ID: mdl-35110408

ABSTRACT

Domoic acid (DA), the causative agent of amnesic shellfish poisoning, is produced by select organisms within two distantly related algal clades: planktonic diatoms and red macroalgae. The biosynthetic pathway to isodomoic acid A was recently solved in the harmful algal bloom-forming diatom Pseudonitzschia multiseries, establishing the genetic basis for the global production of this potent neurotoxin. Herein, we sequenced the 507-Mb genome of Chondria armata, the red macroalgal seaweed from which DA was first isolated in the 1950s, identifying several copies of the red algal DA (rad) biosynthetic gene cluster. The rad genes are organized similarly to the diatom DA biosynthesis cluster in terms of gene synteny, including a cytochrome P450 (CYP450) enzyme critical to DA production that is notably absent in red algae that produce the simpler kainoid neurochemical, kainic acid. The biochemical characterization of the N-prenyltransferase (RadA) and kainoid synthase (RadC) enzymes support a slightly altered DA biosynthetic model in C. armata via the congener isodomoic acid B, with RadC behaving more like the homologous diatom enzyme despite higher amino acid similarity to red algal kainic acid synthesis enzymes. A phylogenetic analysis of the rad genes suggests unique origins for the red macroalgal and diatom genes in their respective hosts, with native eukaryotic CYP450 neofunctionalization combining with the horizontal gene transfer of N-prenyltransferases and kainoid synthases to establish DA production within the algal lineages.


Subject(s)
Dimethylallyltranstransferase/genetics , Dimethylallyltranstransferase/metabolism , Kainic Acid/analogs & derivatives , Neurotoxins/metabolism , Rhodophyta/metabolism , Biological Evolution , Biosynthetic Pathways/genetics , Diatoms/genetics , Diatoms/metabolism , Harmful Algal Bloom/physiology , Kainic Acid/metabolism , Multigene Family/genetics , Neurotoxins/genetics , Phylogeny , Shellfish Poisoning/metabolism
12.
Environ Microbiol ; 26(1): e16564, 2024 Jan.
Article in English | MEDLINE | ID: mdl-38151764

ABSTRACT

Different marine seaweed species have been shown to harbour specific bacterial communities, however, the extent to which vertical symbiont transmission from parents to offspring contributes to host-specificity is unclear. Here we use fluorescence and electron microscopy as well as 16S rRNA gene-based community analysis to investigate symbiont transmission in members of the three major seaweed groups (green Chlorophyta, red Rhodophyta and brown Phaeophyceae). We found seaweeds employ diverse strategies to transfer symbionts to their progeny. For instance, the green Ulva australis does not appear to have the capacity for vertical transmission. In contrast, the brown Phyllospora comosa adopts a non-selective vertical transmission. The red Delisea pulchra demonstrates weak selectivity in symbiont transmission, while the brown Hormosira banksii exhibits a strongly selective symbiont transfer. Mucilage on the gametes appears to facilitate vertical transmission and transferred bacteria have predicted properties that could support early development of the seaweeds. Previous meta-analysis has indicated that vertical transmission is rare in aquatic compared to terrestrial environments, however, our results contribute to the growing evidence that this might not be the case and that instead vertical transmission with various degrees of symbiont selection occurs in the ecologically important group of seaweeds.


Subject(s)
Chlorophyta , Phaeophyceae , Rhodophyta , Seaweed , RNA, Ribosomal, 16S/genetics , Seaweed/microbiology , Rhodophyta/microbiology , Chlorophyta/genetics , Bacteria/genetics
13.
Environ Microbiol ; 26(5): e16629, 2024 May.
Article in English | MEDLINE | ID: mdl-38695111

ABSTRACT

Horizontal genetic transfer (HGT) is a common phenomenon in eukaryotic genomes. However, the mechanisms by which HGT-derived genes persist and integrate into other pathways remain unclear. This topic is of significant interest because, over time, the stressors that initially favoured the fixation of HGT may diminish or disappear. Despite this, the foreign genes may continue to exist if they become part of a broader stress response or other pathways. The conventional model suggests that the acquisition of HGT equates to adaptation. However, this model may evolve into more complex interactions between gene products, a concept we refer to as the 'Integrated HGT Model' (IHM). To explore this concept further, we studied specialized HGT-derived genes that encode heavy metal detoxification functions. The recruitment of these genes into other pathways could provide clear examples of IHM. In our study, we exposed two anciently diverged species of polyextremophilic red algae from the Galdieria genus to arsenic and mercury stress in laboratory cultures. We then analysed the transcriptome data using differential and coexpression analysis. Our findings revealed that mercury detoxification follows a 'one gene-one function' model, resulting in an indivisible response. In contrast, the arsH gene in the arsenite response pathway demonstrated a complex pattern of duplication, divergence and potential neofunctionalization, consistent with the IHM. Our research sheds light on the fate and integration of ancient HGTs, providing a novel perspective on the ecology of extremophiles.


Subject(s)
Arsenic , Extremophiles , Gene Transfer, Horizontal , Rhodophyta , Rhodophyta/genetics , Extremophiles/genetics , Arsenic/metabolism , Mercury/metabolism , Stress, Physiological/genetics , Inactivation, Metabolic/genetics , Evolution, Molecular
14.
Annu Rev Genet ; 50: 133-154, 2016 Nov 23.
Article in English | MEDLINE | ID: mdl-27617970

ABSTRACT

The life cycles of eukaryotes alternate between haploid and diploid phases, which are initiated by meiosis and gamete fusion, respectively. In both ascomycete and basidiomycete fungi and chlorophyte algae, the haploid-to-diploid transition is regulated by a pair of paralogous homeodomain protein encoding genes. That a common genetic program controls the haploid-to-diploid transition in phylogenetically disparate eukaryotic lineages suggests this may be the ancestral function for homeodomain proteins. Multicellularity has evolved independently in many eukaryotic lineages in either one or both phases of the life cycle. Organisms, such as land plants, exhibiting a life cycle whereby multicellular bodies develop in both the haploid and diploid phases are often referred to as possessing an alternation of generations. We review recent progress on understanding the genetic basis for the land plant alternation of generations and highlight the roles that homeodomain-encoding genes may have played in the evolution of complex multicellularity in this lineage.


Subject(s)
Biological Evolution , Plants/genetics , Bryophyta/genetics , Chlorophyta/genetics , Diploidy , Eukaryota , Fungi/genetics , Haploidy , Homeodomain Proteins/genetics , Magnoliopsida/genetics , Phaeophyceae/genetics , Phylogeny , Rhodophyta/genetics
15.
Proc Biol Sci ; 291(2023): 20240623, 2024 May.
Article in English | MEDLINE | ID: mdl-38807518

ABSTRACT

Intraspecific and habitat-mediated responses to chemical cues play key roles in structuring populations of marine species. We investigated the behaviour of herbivorous-stage juvenile crown-of-thorns sea stars (COTS; Acanthaster sp.) in flow-through choice chambers to determine if chemical cues from their habitat influence movement and their transition to become coral predators. Juveniles at the diet transition stage were exposed to cues from their nursery habitat (coral rubble-crustose coralline algae (CCA)), live coral and adult COTS to determine if waterborne cues influence movement. In response to CCA and coral as sole cues, juveniles moved towards the cue source and when these cues were presented in combination, they exhibited a preference for coral. Juveniles moved away from adult COTS cues. Exposure to food cues (coral, CCA) in the presence of adult cues resulted in variable responses. Our results suggest a feedback mechanism whereby juvenile behaviour is mediated by adult chemical cues. Cues from the adult population may deter juveniles from the switch to corallivory. As outbreaks wane, juveniles released from competition may serve as a proximate source of outbreaks, supporting the juveniles-in-waiting hypothesis. The accumulation of juveniles within the reef infrastructure is an underappreciated potential source of COTS outbreaks that devastate coral reefs.


Subject(s)
Anthozoa , Cues , Starfish , Animals , Anthozoa/physiology , Starfish/physiology , Coral Reefs , Herbivory , Ecosystem , Feeding Behavior , Rhodophyta/physiology
16.
Appl Environ Microbiol ; 90(1): e0170423, 2024 01 24.
Article in English | MEDLINE | ID: mdl-38169280

ABSTRACT

Catabolism of algal polysaccharides by marine bacteria is a significant process of marine carbon cycling. ß1,3/1,4-Mixed-linkage xylan (MLX) is a class of xylan in the ocean, widely present in the cell walls of red algae. However, the catabolic mechanism of MLX by marine bacteria remains elusive. Recently, we found that a marine Bacteroidetes strain, Polaribacter sp. Q13, is a specialist in degrading MLX, which secretes a novel MLX-specific xylanase. Here, the catabolic specialization of strain Q13 to MLX was studied by multiomics and biochemical analyses. Strain Q13 catabolizes MLX with a canonical starch utilization system (Sus), which is encoded by a single xylan utilization locus, XUL-Q13. In this system, the cell surface glycan-binding protein SGBP-B captures MLX specifically, contributing to the catabolic specificity. The xylanolytic enzyme system of strain Q13 is unique, and the enzymatic cascade dedicates the stepwise hydrolysis of the ß1,3- and ß1,4-linkages in MLX in the extracellular, periplasmic, and cytoplasmic spaces. Bioinformatics analysis and growth observation suggest that other marine Bacteroidetes strains harboring homologous MLX utilization loci also preferentially utilize MLX. These results reveal the catabolic specialization of MLX degradation by marine Bacteroidetes, leading to a better understanding of the degradation and recycling of MLX driven by marine bacteria.IMPORTANCERed algae contribute substantially to the primary production in marine ecosystems. The catabolism of red algal polysaccharides by marine bacteria is important for marine carbon cycling. Mixed-linkage ß1,3/1,4-xylan (MLX, distinct from hetero-ß1,4-xylans from terrestrial plants) is an abundant red algal polysaccharide, whose mechanism of catabolism by marine bacteria, however, remains largely unknown. This study reveals the catabolism of MLX by marine Bacteroidetes, promoting our understanding of the degradation and utilization of algal polysaccharides by marine bacteria. This study also sets a foundation for the biomass conversion of MLX.


Subject(s)
Flavobacteriaceae , Rhodophyta , Xylans/metabolism , Ecosystem , Flavobacteriaceae/metabolism , Polysaccharides/metabolism , Bacteroidetes/metabolism , Plants/metabolism , Rhodophyta/metabolism , Carbon/metabolism
17.
Photosynth Res ; 159(2-3): 165-175, 2024 Mar.
Article in English | MEDLINE | ID: mdl-37233900

ABSTRACT

In response to fluctuation in light intensity and quality, oxygenic photosynthetic organisms modify their light-harvesting and excitation energy-transfer processes to maintain optimal photosynthetic activity. Glaucophytes, which are a group of primary symbiotic algae, possess light-harvesting antennas called phycobilisomes (PBSs) consistent with cyanobacteria and red algae. However, compared with cyanobacteria and red algae, glaucophytes are poorly studied and there are few reports on the regulation of photosynthesis in the group. In this study, we examined the long-term light adaptation of light-harvesting functions in a glaucophyte, Cyanophora paradoxa, grown under different light conditions. Compared with cells grown under white light, the relative number of PBSs to photosystems (PSs) increased in blue-light-grown cells and decreased in green-, yellow-, and red-light-grown cells. Moreover, the PBS number increased with increment in the monochromatic light intensity. More energy was transferred from PBSs to PSII than to PSI under blue light, whereas energy transfer from PBSs to PSII was reduced under green and yellow lights, and energy transfer from the PBSs to both PSs decreased under red light. Decoupling of PBSs was induced by intense green, yellow, and red lights. Energy transfer from PSII to PSI (spillover) was observed, but the contribution of the spillover did not distinctly change depending on the culture light intensity and quality. These results suggest that the glaucophyte C. paradoxa modifies the light-harvesting abilities of both PSs and excitation energy-transfer processes between the light-harvesting antennas and both PSs during long-term light adaption.


Subject(s)
Cyanobacteria , Cyanophora , Rhodophyta , Cyanophora/metabolism , Phycobilisomes/metabolism , Photosynthesis , Cyanobacteria/metabolism , Rhodophyta/metabolism , Energy Transfer , Adaptation, Ocular , Photosystem I Protein Complex/metabolism
18.
Mol Phylogenet Evol ; 197: 108106, 2024 Aug.
Article in English | MEDLINE | ID: mdl-38750675

ABSTRACT

The Hildenbrandiales, a typically saxicolous red algal order, is an early diverging florideophycean group with global significance in marine and freshwater ecosystems across diverse temperature zones. To comprehensively elucidate the diversity, phylogeny, biogeography, and evolution of this order, we conducted a thorough re-examination employing molecular data derived from nearly 700 specimens. Employing a species delimitation method, we identified Evolutionary Species Units (ESUs) within the Hildenbrandiales aiming to enhance our understanding of species diversity and generate the first time-calibrated tree and ancestral area reconstruction for this order. Mitochondrial cox1 and chloroplast rbcL markers were used to infer species boundaries, and subsequent phylogenetic reconstructions involved concatenated sequences of cox1, rbcL, and 18S rDNA. Time calibration of the resulting phylogenetic tree used a fossil record from a Triassic purportedly freshwater Hildenbrandia species and three secondary time points from the literature. Our species delimitation analysis revealed an astounding 97 distinct ESUs, quintupling the known diversity within this order. Our time-calibration analysis placed the origin of Hildenbrandiales (crown age) in the Ediacaran period, with freshwater species emerging as a monophyletic group during the later Permian to early Triassic. Phylogenetic reconstructions identified seven major clades, experiencing early diversification during the Silurian to Carboniferous period. Two major evolutionary events-colonization of freshwater habitats and obligate systemic symbiosis with a marine fungus-marked this order, leading to significant morphological alterations without a commensurate increase in species diversification. Despite the remarkable newly discovered diversity, the extant taxon diversity appears relatively constrained when viewed against an evolutionary timeline spanning over 800 million years. This limitation may stem from restricted geographic sampling or the prevalence of asexual reproduction. However, species richness estimation and rarefaction analyses suggest a substantially larger diversity yet to be uncovered-potentially four times greater. These findings drastically reshape our understanding of the deeply diverging florideophycean order Hildenbrandiales species diversity, and contribute valuable insights into this order's evolutionary history and ecological adaptations. Supported by phylogenetic, ecological and morphological evidence, we established the genus Riverina gen. nov. to accommodate freshwater species of Hildenbrandiales, which form a monophyletic clade in our analyses. This marks the first step toward refining the taxonomy of the Hildenbrandiales, an order demanding thorough revisions, notably with the creation of several genera to address the polyphyletic status of Hildenbrandia. However, the limited diagnostic features pose a challenge, necessitating a fresh approach to defining genera. A potential solution lies in embracing a molecular systematic perspective, which can offer precise delineations of taxonomic boundaries.


Subject(s)
Phylogeny , Rhodophyta , Symbiosis , Symbiosis/genetics , Rhodophyta/genetics , Rhodophyta/classification , Phylogeography , Rivers , Sequence Analysis, DNA , Bayes Theorem , Biodiversity , Evolution, Molecular , Biological Evolution , RNA, Ribosomal, 18S/genetics
19.
Glob Chang Biol ; 30(5): e17300, 2024 May.
Article in English | MEDLINE | ID: mdl-38738563

ABSTRACT

Rhodoliths built by crustose coralline algae (CCA) are ecosystem engineers of global importance. In the Arctic photic zone, their three-dimensional growth emulates the habitat complexity of coral reefs but with a far slower growth rate, growing at micrometers per year rather than millimeters. While climate change is known to exert various impacts on the CCA's calcite skeleton, including geochemical and structural alterations, field observations of net growth over decade-long timescales are lacking. Here, we use a temporally explicit model to show that rising ocean temperatures over nearly 100 years were associated with reduced rhodolith growth at different depths in the Arctic. Over the past 90 years, the median growth rate was 85 µm year-1 but each °C increase in summer seawater temperature decreased growth by a mean of 8.9 µm (95% confidence intervals = 1.32-16.60 µm °C-1, p < .05). The decrease was expressed for rhodolith occurrences in 11 and 27 m water depth but not at 46 m, also having the shortest time series (1991-2015). Although increasing temperatures can spur plant growth, we suggest anthropogenic climate change has either exceeded the population thermal optimum for these CCA, or synergistic effects of warming, ocean acidification, and/or increasing turbidity impair rhodolith growth. Rhodoliths built by calcitic CCA are important habitat providers worldwide, so decreased growth would lead to yet another facet of anthropogenic habitat loss.


Subject(s)
Climate Change , Rhodophyta , Temperature , Arctic Regions , Rhodophyta/growth & development , Rhodophyta/physiology , Seawater/chemistry
20.
Crit Rev Biotechnol ; 44(3): 462-476, 2024 May.
Article in English | MEDLINE | ID: mdl-36842998

ABSTRACT

Nature derived compounds represent a valuable source of bioactive molecules with enormous potential. The sea is one of the richest environments, full of skilled organisms, where algae stand out due to their unique characteristics. Marine macroalgae adapt their phenotypic characteristics, such as chemical composition, depending on the environmental conditions where they live. The compounds produced by these organisms show tremendous potential to be used in the biomedical field, due to their antioxidant, anti-inflammatory, immunomodulatory, and anti-cancer properties.Cancer is one of the deadliest diseases in the world, and the lack of effective treatments highlights the urgent need for the development of new therapeutic strategies. This review provides an overview of the current advances regarding the anti-cancer activity of the three major groups of marine macroalgae, i.e., red algae (Rhodophyta), brown algae (Phaeophyceae), and green algae (Chlorophyta) on pancreatic, lung, breast, cervical, colorectal, liver, and gastric cancers as well as leukemia and melanoma. In addition, future perspectives, and limitations regarding this field of work are also discussed.


Subject(s)
Chlorophyta , Phaeophyceae , Rhodophyta , Seaweed , Rhodophyta/chemistry , Antioxidants/pharmacology , Antioxidants/therapeutic use
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