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Modeling the ecology of parasitic plasmids.

ABSTRACT: Plasmids are autonomous genetic elements that can be exchanged between microorganisms via horizontal gene transfer (HGT). Despite the central role they play in antibiotic resistance and modern biotechnology, our understanding of plasmids' natural ecology is limited. Recent experiments have shown that plasmids can spread even when they are a burden to the cell, suggesting that natural plasmids may exist as parasites. Here, we use mathematical modeling to explore the ecology of such parasitic plasmids. We first develop models of single plasmids and find that a plasmid's population dynamics and optimal infection strategy are strongly determined by the plasmid's HGT mechanism. We then analyze models of co-infecting plasmids and show that parasitic plasmids are prone to a "tragedy of the commons" in which runaway plasmid invasion severely reduces host fitness. We propose that this tragedy of the commons is averted by selection between competing populations and demonstrate this effect in a metapopulation model. We derive predicted distributions of unique plasmid types in genomes-comparison to the distribution of plasmids in a collection of 17,725 genomes supports a model of parasitic plasmids with positive plasmid-plasmid interactions that ameliorate plasmid fitness costs or promote the invasion of new plasmids.

SUBMITTER: Lopez JG

PROVIDER: S-EPMC8443676 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Disease ecology is a rapidly growing subdiscipline, and mammals and their parasites feature prominently in both historical and more recent research efforts. Nevertheless, the diversity of topics explored, and those not well explored, has not been systematically assessed. We conducted a systematic review of the published scientific literature in disease ecology of mammals and subjected the collection of original and review articles identified to a topic modeling approach, which is based on the words used in the published texts and their contexts (i.e., the frequency and strength of their semantic relationships with one another). In addition to concept maps identifying the most prominent research themes, we identified eight (not mutually exclusive) subcategories of studies, including experimental, theoretical, comparative, behavioral, immunological-microbiological, biogeographic-macroecological, vector-focused (e.g., mosquitoes), and disturbance-focused. The most prominent themes arising in review papers included the ecology of zoonotic diseases transmitted from non-human mammals, comparisons of pathogen prevalence between mammalian species, and pathogen discovery-disease surveillance studies, particularly of marine mammals and bats. For the original articles, the most prominent themes included ecology of rodent-transmitted viral and bacterial diseases and the population biology of zoonotic hosts. Most studies used comparative or descriptive approaches to investigate mammal-pathogen-disease relationships at a local scale, focusing on vector-borne diseases. Experimental, modeling, immunological, and behavioral approaches were strikingly underrepresented. Topics of strong conceptual importance, but that are underrepresented in the current literature, include: 1) the effects of the population density of mammalian hosts, and manipulations of density, on pathogen transmission; 2) macroecological studies that quantify effects of mammalian host species on parasite abundance and prevalence; and 3) effects of climate change on physiological and behavioral processes relevant to mammal-parasite interactions.

Project description:Blastodinium is a genus of dinoflagellates that live as parasites in the gut of marine, planktonic copepods in the World's oceans and coastal waters. The taxonomy, phylogeny, and physiology of the genus have only been explored to a limited degree and, based on recent investigations, we hypothesize that the morphological and genetic diversity within this genus may be considerably larger than presently recognized. To address these issues, we obtained 18S rDNA and ITS gene sequences for Blastodinium specimens of different geographical origins, including representatives of the type species. This genetic information was in some cases complemented with new morphological, ultrastructural, physiological, and ecological data. Because most current knowledge about Blastodinium and its effects on copepod hosts stem from publications more than half a century old, we here summarize and discuss the existing knowledge in relation to the new data generated. Most Blastodinium species possess functional chloroplasts, but the parasitic stage, the trophocyte, has etioplasts and probably a limited photosynthetic activity. Sporocytes and swarmer cells have well-developed plastids and plausibly acquire part of their organic carbon needs through photosynthesis. A few species are nearly colorless with no functional chloroplasts. The photosynthetic species are almost exclusively found in warm, oligotrophic waters, indicating a life strategy that may benefit from copepods as microhabitats for acquiring nutrients in a nutrient-limited environment. As reported in the literature, monophyly of the genus is moderately supported, but the three main groups proposed by Chatton in 1920 are consistent with molecular data. However, we demonstrate an important genetic diversity within the genus and provide evidences for new groups and the presence of cryptic species. Finally, we discuss the current knowledge on the occurrence of Blastodinium spp. and their potential impact on natural copepod populations.

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Modeling the ecology of parasitic plasmids.

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