Sebastian D. Fugmann

Inflammation is widely considered a hallmark of animal immune responses. In mammals, this process is mediated in part by pro-inflammatory cytokines of the interleukin 1 (IL-1) superfamily, which establish and support microenvironments that regulate immune cell activity. However, the evolutionary origins of IL-1 cytokines remain elusive, as homologous proteins have been difficult to confidently identify outside vertebrates using sequence-based approaches. Although IL-1 family members have been described in all vertebrate lineages, including cartilaginous and jawless fishes, their distribution and evolutionary relationships beyond these groups remain unclear. Here we applied protein structure prediction algorithms to identify genes encoding a previously unrecognized family of IL-1 proteins (termed ‘IL-1anc’ to reflect their ancestral evolutionary origin) with homologues throughout Eumetazoa. Here, using Petromyzon marinus (sea lamprey) and Strongylocentrotus purpuratus (purple sea urchin) as model systems, we demonstrate that IL-1anc proteins share key features with mammalian IL-1α/IL-1β, including expression patterns, subcellular localization and post-translational processing. Together with previous evidence identifying other IL-1 axis components in invertebrates, our data support a model in which the IL-1 superfamily and associated circuitry represent a foundational module of animal immunity that far predates the jawed vertebrates.

Summary: Inflammation is a hallmark of immune responses. Its mechanistic underpinnings in mammals are well-defined: pro-inflammatory cytokines of the interleukin 1 (IL-1) superfamily establish and support microenvironments that promote immune cell activities. Despite a growing number of reports on inflammatory processes and components of the IL-1 signaling axis in several invertebrate lineages, orthologs of these central cytokines have not been detected outside of the jawed vertebrates. Here, protein structure prediction algorithms were applied to identify genes encoding a family of IL-1 proteins with homologs throughout Eumetazoa (termed “IL-1anc” to reflect their ancestral evolutionary origin). Using Petromyzon marinus (sea lamprey) and Strongylocentrotus purpuratus (purple sea urchin) as model systems, we demonstrate that IL-1anc proteins share important features with mammalian IL-1α/IL-1β including expression patterns, protein localization, and processing. Together, our data indicate that the IL-1 superfamily and associated circuitry represent a foundational module of animal immunity that far predates the jawed vertebrates.

Polylactic acid (PLA), the most popular bioplastic, has high sustainability potential as it is bio-sourced and also harbors biodegradability. A form of its biodegradability is via composting, and it was previously established that thermophilic temperatures are needed for PLA breakdown in composts. Here we report the development of composts that have overcome the temperature requirement needed for PLA composting. Our mesophilic composts exhibited clear PLA biodegradability, and this is due to specific biological activity enriched in our material. To investigate the nature of this mesophilic activity, we conducted metagenomics analysis to reveal the microbial composition and enzyme-coding potential associated with PLA biodegradation. These efforts revealed multiple enzyme subtypes with strong enrichment on PLA surfaces in our trained composts, and the top candidate was a type of hydro-lyase, an enzyme that can cleave carbon-carbon and carbon-oxygen bonds, both present in the chemical structure of PLA, in the absence of water. Hydro-lyases represent a novel class of enzymes that could facilitate PLA degradation, and our results point to the model that the combinatorial action of multiple types of enzymes is what drives PLA biodegradation and how the temperature barrier for PLA composting is overcome.

Oncorhynchus masou formosanus (Formosa landlocked salmon) is a salmonid fish endemic to Taiwan with a critically endangered extant small population in high-altitude mountain streams. To begin to assess the remaining genetic diversity we characterized the single classical MHC class I ( UBA ) and MHC class II ( DAA and DAB ) genes of teleost fish in a small cohort of eight unrelated O. m. formosanus individuals. We focused on the exons encoding the peptide binding regions of these complexes as they are considered the most highly polymorphic regions in vertebrate genomes. Surprisingly, the DAA and DAB genes appeared homozygous and identical among all eight fish indicating that the encoded class II complex is monomorphic. In contrast, three distinct UBA alleles were discovered with one dominant allele present in every single individual. Notably, 75% were heterozygous indicating a selective advantage of heterozygosity at this locus. Lastly, our MHC alleles differ from those present in the genome of the closely related Japanese O. m. masou , suggesting that the loss of DAA/DAB diversity and the emergence of the dominant UBA allele occurred after their populations were isolated. Together we discovered residual genetic diversity at the classical MHC class I locus in O. m. formosanus and maintaining this allelic variation unlike the homozygous DAA and DAB genes is likely important for its survival in its geographically restricted unique habitat.

Embryonic germ cells develop rapidly to establish the foundation for future developmental trajectories, and in this process, they make critical lineage choices including the configuration of their unique identity and a decision on sex. Here, we use single-cell genomics patterns for the entire embryonic germline inDrosophila melanogasteralong with the somatic gonadal precursors after embryonic gonad coalescence to investigate molecular mechanisms involved in the setting up and regulation of the germline program. Profiling of the early germline chromatin landscape revealed sex- and stage-specific features. In the male germline immediately after zygotic activation, the chromatin structure underwent a brief remodeling phase during which nucleosome density was lower and deconcentrated from promoter regions. These findings echoed enrichment analysis results of our genomics data in which top candidates were factors with the ability to mediate large-scale chromatin reorganization. Together, they point to the importance of chromatin regulation in the early germline and raise the possibility of a conserved epigenetic reprogramming-like process required for proper initiation of germline development.

Oncorhynchus masou formosanus (Formosa land-locked salmon) is a critically endangered salmonid fish endemic to Taiwan. To begin to understand how its drastic change in lifestyle from anadromous to exclusively river-dwelling is reflected in its immune genes, we characterized the genes encoding six cytokines (IL-2A, IL-2B, IL-4A, IL-4B1, IL-4B2, and IL-17A/F2a) important for T cell responses as no genomic data is available for this fish. Interestingly, all genes appeared homozygous indicative of a genetic bottleneck. The IL2 and IL17A/F2a genes and their products are highly similar to their characterized homologs in Oncorhynchus mykiss (rainbow trout) and other salmonid fish. Two notable differences were observed in IL4 family important for type 2 immune responses. First, O. m. formosanus carries not only one but two genes encoding IL-4B1 proteins and expansions of these genes are present in other salmonid fish. Second, the OmfoIL4A gene carries a 228 bp deletion that results in a premature stop codon and hence a non-functional IL-4A cytokine. This suggests a reduced ability for T cell responses against parasitic infections in this species.

One of the most promising strategies for the management of plastic waste is microbial biodegradation, but efficient degraders for many types of plastics are still lacking, including those for polystyrene (PS). Genomics has emerged as a powerful tool for mining environmental microbes that may have the ability to degrade different types of plastics. In this study, we use 16S rRNA sequencing to analyze the microbiomes for multiple PS samples collected from sites with different vegetation in Taiwan to reveal potential common properties between species that exhibit growth advantages on PS surfaces. Phylum enrichment analysis identified Cyanobacteria and Deinococcus-Thermus as being the most over-represented groups on PS, and both phyla include species known to reside in extreme environments and could encode unique enzymes that grant them properties suitable for colonization on PS surfaces. Investigation of functional enrichment using reference genomes of PS-enriched species highlighted carbon metabolic pathways, especially those related to hydrocarbon degradation. This is corroborated by the finding that genes encoding long-chain alkane hydroxylases such as AlmA are more prevalent in the genomes of PS-associated bacteria. Our analyses illustrate how plastic in the environment support the colonization by different microbes compared to surrounding soil. In addition, our results point to the possibility that alkane hydroxylases could confer growth advantages of microbes on PS.

One of the most promising strategies for the management of plastic waste is microbial biodegradation, but efficient degraders for many types of plastics are still lacking, including for polystyrene (PS). Genomics has emerged as a powerful tool for mining environmental microbes that may have the ability to degrade different types of plastics. In this study, we use 16S sequencing to analyze the microbiomes for multiple PS samples collected from sites with different vegetation in Taiwan to reveal potential common properties between species that have exhibit growth advantages on PS surfaces. Phylum enrichment analysis identified Cyanobacteria and Deinococcus-Thermus as being the most over-represented groups on PS, and both phyla include species known to reside in extreme environments and could encode unique enzymes that grant them properties suitable for colonization on PS surfaces. Investigation of functional enrichment in PS-enriched species highlighted carbon metabolic pathways, especially those related to hydrocarbon degradation. This is corroborated by the finding that genes encoding long-chain alkane hydroxylases such as AlmA are more prevalent in the genomes of PS-associated bacteria. Our analyses illustrate how plastic in the environment support the colonization of different microbes compared to surrounding soil. In addition, our results point to the possibility that alkane hydroxylases could confer growth advantages of microbes on PS.