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The Reduced Genome of a Heritable Symbiont from an Ectoparasitic Feather Feeding Louse Leila Alickovic1, Kevin P

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The Reduced Genome of a Heritable Symbiont from an Ectoparasitic Feather Feeding Louse Leila Alickovic1, Kevin P Alickovic et al. BMC Ecol Evo (2021) 21:108 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01840-7 RESEARCH Open Access The reduced genome of a heritable symbiont from an ectoparasitic feather feeding louse Leila Alickovic1, Kevin P. Johnson2 and Bret M. Boyd1* Abstract Background: Feather feeding lice are abundant and diverse ectoparasites that complete their entire life cycle on an avian host. The principal or sole source of nutrition for these lice is feathers. Feathers appear to lack four amino acids that the lice would require to complete development and reproduce. Several insect groups have acquired heritable and intracellular bacteria that can synthesize metabolites absent in an insect’s diet, allowing insects to feed exclu- sively on nutrient-poor resources. Multiple species of feather feeding lice have been shown to harbor heritable and intracellular bacteria. We expected that these bacteria augment the louse’s diet with amino acids and facilitated the evolution of these diverse and specialized parasites. Heritable symbionts of insects often have small genomes that contain a minimal set of genes needed to maintain essential cell functions and synthesize metabolites absent in the host insect’s diet. Therefore, we expected the genome of a bacterial endosymbiont in feather lice would be small, but encode pathways for biosynthesis of amino acids. Results: We sequenced the genome of a bacterial symbiont from a feather feeding louse (Columbicola wolfhuegeli) that parasitizes the Pied Imperial Pigeon (Ducula bicolor) and used its genome to predict metabolism of amino acids based on the presence or absence of genes. We found that this bacterial symbiont has a small genome, similar to the genomes of heritable symbionts described in other insect groups. However, we failed to identify many of the genes that we expected would support metabolism of amino acids in the symbiont genome. We also evaluated other gene pathways and features of the highly reduced genome of this symbiotic bacterium. Conclusions: Based on the data collected in this study, it does not appear that this bacterial symbiont can synthesize amino acids needed to complement the diet of a feather feeding louse. Our results raise additional questions about the biology of feather chewing lice and the roles of symbiotic bacteria in evolution of diverse avian parasites. Keywords: Phthiraptera, Endosymbiont, Keratin, Genome reduction, Metabolic complementation Background known as host-benefcial endosymbionts [4, 5]. Some Insects require an exogenous source of macro- and insects that parasitize plants and vertebrate animals micronutrients to complete development and reproduce are dependent on microbes for nutrients [6–8]. Tis is [1–3]. Tese nutrients are obtained from the insect’s diet because parasites often possess specialized morphology [1–3] or from microbes that reside within the insect, that allows them to exploit host resources; however, these morphological adaptations prevent the parasites from utilizing other resources. While a host resource may be *Correspondence: [email protected] 1 Center for the Study of Biological Complexity, Virginia Commonwealth rich in many nutrients, it may lack one or a few nutrients University, 1000 W. Cary St., Suite 111, Richmond, VA 23284-2030, USA that are essential for insect development and benefcial Full list of author information is available at the end of the article microbes can provide these missing nutrients [6, 8]. © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Alickovic et al. BMC Ecol Evo (2021) 21:108 Page 2 of 11 Genome sequencing has advanced investigations of amino acid metabolism, specifcally for metabolisms of insect-microbial symbioses [5]. Up to a third of insect histidine, lysine, methionine, and tryptophan. species are host to benefcial microbes [4, 9]. Many We predicted the amino acid content of feather kera- benefcial microbes identifed within insects are bacte- tin in the rock dove (Aves: Columbifomes: Columba ria [10], and these bacteria often have small genomes, livia) by identifying feather keratin encoding genes in when compared to free-living and pathogenic bacteria the genome of the rock dove and determining the pre- [5]. Tese small genomes contain the genes needed to dicted contribution of each amino acid to the primary complete basic bacterial cellular functions, but also the structure of keratin. We initially considered sequencing metabolic pathways needed to provide the host with and annotating the genome of the benefcial endosym- nutrients absent in the host’s diet [7, 11]. While iden- biont from lice parasitizing the rock dove [21, 22]. How- tifying the genes underlying metabolism in the genome ever, we were concerned that this symbiont’s genome of a symbiotic bacteria would not prove the bacteria are may not be acceptable for testing our hypothesis. Given supplying the host with metabolites, it is a frst step in a few exceptions, endosymbiotic bacteria that possess a identifying a candidate role for these bacteria. Tere- small genome also show a bias in nucleotide base com- fore, we can make predictions and provide an initial position, with adenine–thymine (AT) bases representing test of hypotheses using genome sequencing. the majority of bases [30]. Fukatsu et al. [21] and Smith Tere are approximately 500 species of blood feed- et al. [22] reported sequences for the symbiotic bacte- ing sucking lice (Insecta; Phthiraptera; Anoplura), while ria isolated from lice parasitizing the rock dove. Tese there are over 4500 species of chewing lice (Insecta; sequences were composed of more than 50% guanine- Phthiraptera; Ischnocera and Amblycera) [12, 13]. cytosine base pairs (fusA, 51% GC; groEL 53% GC). In Extensive research has elucidated the roles and his- comparison, the orthologous sequences obtained from tory of bacterial endosymbionts of blood sucking lice the highly reduced genome of the endosymbiont of the [6, 14–19], but much less is known about the closely human head louse (Candidatus Riesia pediculicola) con- related chewing lice. Chewing lice either feed on blood tain a majority of AT base pairs (fusA, 38% GC; groEL, by chewing through a host’s skin [20] or consume der- 35% GC). While insect benefcial endosymbionts have mal elements, such as feathers or sebaceous secretions small genomes, they are believed to have been derived [13]. Most species of chewing lice in the diverse sub- from bacterial with larger genome and that their genomes order Ischnocera parasitize birds and nearly exclusively are reduced after the symbiotic relationship is formed consume feathers [13]. Just like blood feeding lice, sym- [5, 31–33]. A majority GC composition could be associ- biotic bacteria have been identifed in multiple spe- ated with a larger genome that has not been reduced and cies of feather chewing lice (Phthiraptera: Ischnocera: would be poor choice for our study. Columbicola) that parasitize dove and pigeon species During a recent study of pigeon and dove lice [34], we (hereafter doves) [21, 22]. Terefore, dove lice pro- identifed a partial genome assembly from an endosym- vided us with a system to study microbial symbioses in biont that was enriched for AT base pairs and appeared feather chewing lice. well suited for our study. Terefore, we chose to focus on Feather feeding lice primarily consume the barbs of this louse and its endosymbiont with the assumption that downy feathers. Dove lice specifcally ingest feathers the genome would be small and well suited for our study. barbs from feathers found on the abdominal region of Here we present the genome of a symbiotic bacteria iden- birds [23–26] and adult lice can persist in of the body tifed from an ischnoceran feather chewing louse Colum- of the host when provided with appropriate abdominal bicola wolfhuegeli (Phthiraptera: Ischnocera). Tis louse feathers [27]. Feather barbs are composed of keratin, and parasitizes the Pied Imperial Pigeon (Ducula bicolor; analysis of feather keratin from chickens would suggest Aves Columbidae) in Australia. feather keratin lacks four of the 10 amino acids insects require in their diet (histidine, lysine, methionine, and Results tryptophan) [28, 29]. Given that feather chewing lice are To understand the composition of dove feather barbs, we known to harbor endosymbiotic bacteria, we hypoth- used the genome of the rock dove to predict the amino esized that they might provide the lice with a source of acid composition of feather keratin. We evaluated our these four amino acids. In this study we did two things predictive process by making the same predictions of to address this hypothesis. (1) We predicted amino acid amino acid composition of feather keratins in the chicken composition of feather keratin from a dove species. (2) (Gallus gallus) and then compared the results to known We used genome sequencing and annotation to deter- feather keratin amino acid composition as determined by mine if a symbiotic bacterium from a feather chewing Arai et al.
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