Biology subjects

Berasategui, A.

Publications and source records attributed to Berasategui, A..

6 recordsLinked to original sources

bioRxiv2025

Comparative genomics of Sympodiorosea identifies genome evolution mediated through selective pressure on the metabolic gene repertoire

Biological interactions involving host-associated fungi are manifestations of chemistry shaped over evolutionary time. For antagonistic fungi, specialization to host fungi is often facilitated through the acquisition of genes encoding novel secretions, including proteins and specialized metabolites that shape interactions with host defenses, as well the acquisition of nutrients. Alternatively, novel function may arise from diversifying selection eliciting evolutionary innovation in inert secretions. Through specialization, fungal metabolic capacity can serve as an imprint of the selective forces imposed on the antagonist and provide insights into its natural history and occupied niche. Here, we conduct a phylogenomic investigation of antagonistic ascomycetes in the genus Sympodiorosea, which are commonly found in basal fungus-growing ant gardens. Sympodiorosea and closely related genera of Escovopsis, Luteomyces, and Escovopsioides are canonically referenced as virulent mycoparasites, however, recent work has illuminated the possibility for diverse, non-virulent species to emerge within these attine-associated fungi. We explored genomic variation in Sympodiorosea to gain insight into the genomic potential for alternative lifestyles, focusing on diversity and evolution of metabolic genes. Our study revealed a constrained selective landscape across the Sympodiorosea genome. However, outcomes of in vitro interactions with host fungi are diverse and predictable based on the antagonists ant-species-of-origin, suggesting functional diversification. Phylogenomics reveals that gain/loss events of genes involved in secretions (secretome) are potential drivers of diversification. Additionally, we demonstrate that purifying selection acts more intensely on secretome-related genes relative to other genes. In contrast, few genes from the secretome experience diversifying selection, suggesting a mechanistic role for driving both functional differences between strains and host-specialization. Comparative genomics including other fungi within the family Hypocreales reveals that Sympodiorosea has experienced expansions and contractions in proteases genes that are discordant from expectations under a strictly mycoparasitic lifestyle, indicating either the potential for an alternative lifestyle within ant gardens, or that Sympodiorosea recently evolved from other niches. These results provide novel insight into genomic evolution of these fungi and inform future experimental studies of the ecology and chemistry of interactions within the complex fungus-growing ant symbiosis.

evolutionary biology↗

bioRxiv2023

Paleocene origin of a streamlined digestive symbiosis in leaf beetles

Timing the acquisition of a beneficial microbe relative to the evolutionary history of its host can shed light on the adaptive impact of a partnership. Here, we investigated the onset and molecular evolution of an obligate symbiosis between Cassidinae leaf beetles and Candidatus Stammera capleta, a {gamma}-proteobacterium. Residing extracellularly within foregut symbiotic organs, Stammera upgrades the digestive physiology of its host by supplementing plant cell wall-degrading enzymes. We observe that Stammera is a shared symbiont across tortoise and hispine beetles that collectively comprise the Cassidinae subfamily, despite differences in their folivorous habits. In contrast to its transcriptional profile during vertical transmission, Stammera elevates the expression of genes encoding digestive enzymes while in the foregut symbiotic organs, matching the nutritional requirements of its host. Symbiont acquisition during the Paleocene ([~]62 Mya) did not coincide with the origin of Cassidinae beetles, despite the widespread distribution of Stammera across the subfamily. Early-diverging lineages lack the symbiont and the specialized organs that house it. Reconstructing the ancestral state of host-beneficial factors revealed that Stammera encoded three digestive enzymes at the onset of symbiosis, including polygalacturonase - a pectinase that is universally shared. While non-symbiotic cassidines encode polygalacturonase endogenously, their repertoire of plant cell wall-degrading enzymes is more limited compared to symbiotic beetles supplemented with digestive enzymes from Stammera. Highlighting the potential impact of a symbiotic condition and an upgraded metabolic potential, Stammera-harboring beetles exploit a greater variety of plants and are more speciose compared to non-symbiotic members of the Cassidinae.

evolutionary biology↗

bioRxiv2023

Genomic insights into the evolution of secondary metabolism of Escovopsis and its allies, specialized fungal symbionts of fungus-farming ants

The metabolic intimacy of symbiosis often demands the work of specialists. Natural products and defensive secondary metabolites can drive specificity by ensuring infection and propagation across host generations. But in contrast to bacteria, little is known about the diversity and distribution of natural product biosynthetic pathways among fungi and how they evolve to facilitate symbiosis and adaptation to their host environment. In this study, we define the secondary metabolism of Escovopsis and closely related genera, members of which are specialized, diverse ascomycete fungi best known as mycoparasites of the fungal cultivars grown by fungus-growing ants. We ask how the gain and loss of various biosynthetic pathways corresponds to divergent lifestyles. Long-read sequencing allowed us to define the chromosomal features of representative Escovopsis strains, revealing highly reduced genomes (21.4-38.3 Mb) composed of 7-8 chromosomes. Escovopsis genomes are highly co-linear, with genes localizing not only in the same chromosome, but also in the same order. Macrosynteny is high within Escovopsis clades, and decreases with increasing phylogenetic distance, while maintaining a high degree of mesosynteny. To explore the evolutionary history of biosynthetic pathways in this group of symbionts relative to their encoding lineages, we performed an ancestral state reconstruction analysis, which revealed that, while many secondary metabolites are shared with non-ant associated sordariomycetes, 56 pathways are unique to the symbiotic genera. Reflecting adaptation to diverging ant agricultural systems, we observe that the stepwise acquisition of these pathways mirrors the ecological radiations of attine ants and the dynamic recruitment and replacement of their fungal cultivars. As different clades encode characteristic combinations of biosynthetic gene clusters, these delineating profiles provide important insights into the possible mechanisms underlying specificity between these symbionts and their hosts. Collectively, our findings shed light on the evolutionary dynamic nature of secondary metabolism in Escovopsis and its allies, reflecting adaptation of the symbionts to an ancient agricultural system.

evolutionary biology↗

bioRxiv2021

Evaluating the role of coevolution in a horizontally transmitted mutualism

Mutualism depends on the alignment of host and symbiont fitness. Horizontal transmission can readily decouple fitness interests, yet horizontally transmitted mutualisms are common in nature. We hypothesized that pairwise coevolution and specialization in host-symbiont interactions underlies the maintenance of cooperation in a horizontally transmitted mutualism. Alternatively, we predicted selection by multiple host species may select for cooperative traits in a generalist symbiont through diffuse coevolution. We tested for signatures of pairwise coevolutionary change between the squash bug Anasa tristis and its horizontally acquired bacterial symbiont Caballeronia spp. by measuring local adaptation. We found no evidence for local adaptation between sympatric combinations of A. tristis squash bugs and Caballeronia spp. across their native geographic range. To test for diffuse coevolution, we performed reciprocal inoculations to test for specialization between three Anasa host species and Caballeronia spp. symbionts isolated from conspecific hosts. We observed no evidence of specialization across host species. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia spp. symbionts. Specifically, diffuse coevolution between multiple host species with a shared generalist symbiont may maintain cooperative traits despite horizontal transmission.

evolutionary biology↗

bioRxiv2021

The importance of environmentally-acquired bacterial symbionts for the squash bug (Anasa tristis), a significant agricultural pest

Most insects maintain associations with microbes that shape their ecology and evolution. Such symbioses have important applied implications when the associated insects are pests or vectors of disease. The squash bug, Anasa tristis (Coreoidea: Coreidae), is a significant pest of human agriculture in its own right and also causes damage to crops due to its capacity to transmit a bacterial plant pathogen. Here, we demonstrate that complete understanding of these insects requires consideration of their association with bacterial symbionts in the family Burkholderiaceae. Isolation and sequencing of bacteria housed in midgut crypts in these insects indicates that these bacteria are consistent and dominant members of the crypt-associated bacterial communities. These symbionts are closely related to Caballeronia spp. associated other true bugs in the superfamiles Lygaeoidea and Coreoidea. Fitness assays with representative Burkholderiaceae strains indicate that the association can significantly increase survival and decrease development time, though strains do vary in the benefits that they confer to their hosts, with Caballeronia spp. providing the greatest benefit. Experiments designed to assess transmission mode indicate that unlike many other beneficial insect symbionts, the bacteria are not acquired from parents before or after hatching but are instead acquired from the environment after molting to a later development stage. The bacteria do, however, have the capacity to escape adults to be transmitted to later generations, leaving the possibility for a combination of indirect vertical and horizontal transmission.

ecology↗

bioRxiv2017

Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness

The pine weevil (Hylobius abietis), a major pest of conifer forests throughout Europe, feeds on the bark and cambium, tissues rich in terpenoid resins that are toxic to many insect herbivores. Here we report the ability of the pine weevil gut microbiota to degrade the diterpene acids of Norway spruce. The diterpene acid levels present in ingested bark were substantially reduced on passage through the pine weevil gut. This reduction was significantly less upon antibiotic treatment, and supplementing the diet with gut suspensions from untreated insects restored the ability to degrade diterpenes. In addition, cultured bacteria isolated from pine weevil guts were shown to degrade a Norway spruce diterpene acid. In a metagenomic survey of the insects bacterial community, we were able to annotate several genes of a previously described diterpene degradation (dit) gene cluster. Antibiotic treatment disrupted the core bacterial community of H. abietis guts and eliminated nearly all dit-genes concordant with its reduction of diterpene degradation. Pine weevils reared on an artificial diet spiked with diterpenes, but without antibiotics, were found to lay more eggs with a higher hatching rate than weevils raised on diets with antibiotics or without diterpenes. These results suggest that gut symbionts contribute towards host fitness, but not by detoxification of diterpenes, since these compounds do not show toxic effects with or without antibiotics. Rather the ability to thrive in a terpene rich environment appears to allow gut microbes to benefit the weevil in other ways, such as increasing the nutritional properties of their diet.

evolutionary biology↗