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Biology subjects

Mohamed, A. R.

Publications and source records attributed to Mohamed, A. R..

8 recordsLinked to original sources

Vitamin B6 Catabolites Act as Interkingdom Signals Within the Marine Microbiome

More than half of all net primary productivity in the oceans is exchanged and recycled among marine microbial communities, through a network of complex interactions that fuel the global carbon cycle and control oceanic biogeochemistry1,2. Cryptic chemical signals control these interactions, thereby governing interspecies metabolite exchanges and structuring the ocean microbiome3. Here, we show that vitamin B6 catabolites--molecules long assumed to be inert byproducts of metabolism--in fact serve as potent, bidirectional, and widely distributed chemical signals that structure metabolite exchanges between marine eukaryotic phytoplankton and bacteria. We demonstrate that a ubiquitous diatom and its bacterial symbiont exchange five intermediates and catabolites in the glycerophospholipid and vitamin B6 metabolic pathways, previously not implicated in interspecies interactions. Acting in combination, these signals induce broad transcriptional responses that prime each organism to anticipate metabolic input from its partner and enter a symbiotic-like state, despite having no measurable effect on growth. We further identify and biochemically validate the enzymes biosynthesizing two of these signals: diatom-derived 4-pyridoxolactone and bacterially-derived 4-pyridoxate--a catabolite long regarded as bacterial waste4. Genes encoding these enzymes are globally distributed and co-expressed across diverse sunlit ocean microbial communities, indicating that vitamin B6-mediated communication is widespread in the ocean. Together, these findings reveal an unexpected signaling role for vitamin B6 and demonstrate that canonical metabolic byproducts can function as information-rich signals structuring interkingdom interactions in the oceans.

microbiology↗

Endozoicomonas provides corals with steroid hormones during thermal stress

The coral microbiome is believed to play a critical role in sustaining corals and enabling adaptation to thermal stress. A ubiquitous group of coral-associated bacteria, known as Endozoicomonas, are hypothesized to provide essential metabolites to corals, though the exact roles these bacteria play during ambient or thermal stress conditions are largely unknown. We demonstrate that while Endozoicomonas synthesizes the iron-binding siderophore aerobactin in vitro, this trait may be suppressed in hospite. Integrated metagenomics, metabolomics, and lab validations reveal that within the coral holobiont Endozoicomonas is the only microbe capable of metabolizing coral-derived testosterone and converting ubiquitous cholesterol into testosterone and progesterone, important steroids that accumulate within the coral holobiont during thermal stress. Provision of testosterone and progesterone to corals during thermal stress induced transcriptional reprogramming of the coral innate immune response, promoting cellular survival and suggesting active microbial involvement in immune priming and stress resilience. These findings highlight a previously unrecognized mechanism of microbial contribution to coral resilience. Lastly, the capacity of bacteria to synthesize eukaryotic steroids implies deep evolutionary connections between microbial metabolism and the origin of steroid-mediated processes in early eukaryogenesis.

microbiology↗

Molecular mechanisms of microbiome modulation by the diatom secondary metabolite azelaic acid

Photosynthetic eukaryotes, such as microalgae and plants, foster fundamentally important relationships with their microbiome based on the reciprocal exchange of chemical currencies. Among these, the dicarboxylate metabolite azelaic acid (Aze) appears to play an important, but heterogeneous, role in modulating these microbiomes, as it is used as a carbon source for some heterotrophs but is toxic to others. However, the ability of Aze to promote or inhibit growth, as well as its uptake and assimilation mechanisms into bacterial cells are mostly unknown. Here, we use transcriptomics, transcriptional factor coexpression networks, uptake experiments, and metabolomics to unravel the uptake, catabolism and toxicity of Aze on two microalgal-associated bacteria, Phycobacter and Alteromonas, whose growth is promoted or inhibited by Aze, respectively. We identify the first putative Aze transporter in bacteria, a C4-TRAP transporter, and show that Aze is assimilated through fatty acid degradation, with further catabolism occurring through the glyoxylate and butanoate metabolism pathways when used as a carbon source. Phycobacter took up Aze at an initial uptake rate of 3.8x10-9 nmol cell-1 hr-1 and utilized it as a carbon source in concentrations ranging from 10 M-1 mM, suggesting a broad range of acclimation to Aze availability. For inhibited bacteria, we infer that Aze inhibits the ribosome and/or protein synthesis and that a suite of efflux pumps is utilized to shuttle Aze outside the cytoplasm. We demonstrate that seawater amended with Aze becomes enriched in bacterial families that can catabolise Aze, which appears to be a different mechanism from that in soil, where modulation by the host plant is required. This study enhances our understanding of carbon cycling in the oceans and how microscale chemical interactions can structure marine microbial populations. In addition, our findings unravel the role of a key chemical currency in the modulation of eukaryote-microbiome interactions across diverse ecosystems.

ecology↗

Ploidy variation and its implications for reproduction and population dynamics in two sympatric Hawaiian coral species

Standing genetic variation is a major driver of fitness and resilience, and therefore of fundamental importance for threatened species such as stony corals. We analyzed RNA- seq data generated from 132 Montipora capitata and 119 Pocillopora acuta coral colonies collected from K[a]neohe Bay, Oahu, Hawaii. Our goals were to determine the extent of colony genetic variation and to study reproductive strategies in these two sympatric species. Surprisingly, we found that 63% of the P. acuta colonies were triploid, with putative independent origins of the different triploid clades. These corals have spread primarily via asexual reproduction and are descended from a small number of genotypes, whose diploid ancestor invaded the bay. In contrast, all M. capitata colonies are diploid, outbreeding, with almost all colonies genetically distinct. Only two cases of asexual reproduction, likely via fragmentation, were identified in this species. We report two distinct strategies in sympatric coral species that inhabit the largest sheltered body of water in the main Hawaiian Islands. These data highlight divergence in reproductive behavior and genome biology, both of which contribute to coral resilience and persistence. Significance StatementGiven the threat posed to coral reef ecosystems by human caused climate change, there is a growing focus on developing strategies for the protection and restoration of these critical marine habitats. These efforts are however limited by our understanding of the diversity of coral survival and reproductive strategies. Our analysis of data from two coral species inhabiting the same Hawaiian bay found that one is a strict sexual outbreeder, whereas the other reproduces predominantly asexually (i.e., clonally) and includes both diploids and triploids. These results broaden our understanding of coral biology, adaptability, and evolution, and underpin future research into the mechanisms of coral resilience that can inform restoration activities.

genomics↗

Close relationships between coral-associated Chromera strains despite differences within the Symbiodiniaceae

Reef-building corals live in a mutualistic relationship with photosynthetic algae (family Symbiodiniaceae) that usually provide most of the energy required by the coral host. This relationship is sensitive to temperature stress; as little as a 1{degrees}C increase often leading to collapse of the association. This sensitivity has led to interest in the potential of more stress tolerant algae to supplement or substitute for the normal Symbiodiniaceae mutualists. In this respect, the apicomplexan-like microalga Chromera is of particular interest due to its greater temperature tolerance. We generated a de novo transcriptome for a Chromera strain isolated from a GBR coral ("GBR Chromera") and compared to those of the reference strain of Chromera ("Sydney Chromera"), and to those of Symbiodiniaceae (Fugacium, Cladocopium and Breviolum), as well as the apicomplexan parasite, Plasmodium falciparum. By contrast with the Symbiodiniaceae, the two Chromera strains had a high level of sequence similarity evident by very low levels of divergence in orthologous genes. Although KEGG categories provide few criteria by which true coral mutualists might be identified, they do supply a molecular rationalization for the ubiquitous association of Cladocopium strains with Indo-Pacific reef corals. The presence of HSP20 genes may underlie the higher thermal tolerance of Chromera.

genomics↗

Genomes of Symbiodiniaceae reveal extensive sequence divergence but conserved functions at family and genus levels

Dinoflagellates of the family Symbiodiniaceae (Order Suessiales) are predominantly symbiotic, and many are known for their association with corals. The genetic and functional diversity among Symbiodiniaceae is well acknowledged, but the genome-wide sequence divergence among these lineages remains little known. Here, we present de novo genome assemblies of five isolates from the basal genus Symbiodinium, encompassing distinct ecological niches. Incorporating existing data from Symbiodiniaceae and other Suessiales (15 genome datasets in total), we investigated genome features that are common or unique to these Symbiodiniaceae, to genus Symbiodinium, and to the individual species S. microadriaticum and S. tridacnidorum. Our whole-genome comparisons reveal extensive sequence divergence, with no sequence regions common to all 15. Based on similarity of k-mers from whole-genome sequences, the distances among Symbiodinium isolates are similar to those between isolates of distinct genera. We observed extensive structural rearrangements among symbiodiniacean genomes; those from two distinct Symbiodinium species share the most (853) syntenic gene blocks. Functions enriched in genes core to Symbiodiniaceae are also enriched in those core to Symbiodinium. Gene functions related to symbiosis and stress response exhibit similar relative abundance in all analysed genomes. Our results suggest that structural rearrangements contribute to genome sequence divergence in Symbiodiniaceae even within a same species, but the gene functions have remained largely conserved in Suessiales. This is the first comprehensive comparison of Symbiodiniaceae based on whole-genome sequence data, including comparisons at the intra-genus and intra-species levels.

genomics↗

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

Symbiodiniaceae are predominantly symbiotic dinoflagellates critical to corals and other reef organisms. Symbiodinium is a basal symbiodiniacean lineage and includes symbiotic and free-living taxa. However, the molecular mechanisms underpinning these distinct lifestyles remain little known. Here, we present high-quality de novo genome assemblies for the symbiotic Symbiodinium tridacnidorum CCMP2592 (genome size 1.3 Gbp) and the free-living Symbiodinium natans CCMP2548 (genome size 0.74 Gbp). These genomes display extensive sequence divergence, sharing only ~1.5% conserved regions ([≥]90% identity). We predicted 45,474 and 35,270 genes for S. tridacnidorum and S. natans, respectively; of the 58,541 homologous gene families, 28.5% are common to both genomes. We recovered a greater extent of gene duplication and higher abundance of repeats, transposable elements and pseudogenes in the genome of S. tridacnidorum than in that of S. natans. These findings demonstrate that genome structural rearrangements are pertinent to distinct lifestyles in Symbiodinium, and may contribute to the vast genetic diversity within the genus, and more broadly in Symbiodiniaceae. Moreover, the results from our whole-genome comparisons against a free-living outgroup support the notion that the symbiotic lifestyle is a derived trait in, and that the free-living lifestyle is ancestral to, Symbiodinium.

genomics↗

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Dinoflagellates are taxonomically diverse, ecologically important phytoplankton in marine and freshwater environments. Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. For each genome, guided using full-length transcriptome data, we predicted >50,000 high-quality genes. About 68% of the genome is repetitive sequence; long terminal repeats likely contribute to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). Of all genes, [~]40% are encoded unidirectionally, [~]25% comprised of single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial, origin of ice-binding domains in cold-adapted dinoflagellates. Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Since most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light environments.

genomics↗