Ecological aspects of the origin of Yersinia pestis,causative agent of the plague: Concept of intermediate environment

Modern phylogenies of Yersinia pestis (Logh.), causative agent of the plague, constructed using molecular-genetic methods, do not receive a satisfactory functional and adaptive interpretation and are far from being ecologically valid. We have presented an ecological scenario of the origin of the causative agent of the plague through the transition of the initial pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b to a free hostal ecological niche (and a new adaptive zone) under ultracontinental climatic conditions of the Late Pleistocene (Sartan time, 22000–15000 years ago) in southern Siberia and Central Asia. An intermediate environment, i.e., the “Mongolian marmot Marmota sibirica-flea Oropsylla silatiewi” parasitic system, where the process of adaptation development of the plague microbe took place, has been characterized. A scenario based on the major principles of the modern synthetic theory of evolution opens the way to an ecological-genetic synthesis of the problem of plague origin and is an appropriate model for developing a theory of molecular evolution of pathogenic (plaguelike) microorganisms.     

Sympatric speciation of the plague microbe <Emphasis Type="Italic">Yersinia pestis</Emphasis>: Monohostal specialization in the host–parasite marmot–flea (<Emphasis Type="Italic">Marmota sibirica–Oropsylla silantiewi</Emphasis>) system

An ecological scenario of the origin of the plague microbe that is interpreted in the light of modern Darwinism (synthetic theory of evolution) is presented. It is shown that the plague microbe emerged from a clone of the psychrophilic saprozoonotic pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b in the mountain steppe landscapes of Central Asia in the Sartan time, 22000–15000 years ago, in the monohostal Mongolian marmot (Marmota sibirica)–flea (Oropsylla silantiewi) host–parasite system. It was noted that the evolutionary process described corresponds to the sympatric form of speciation by transition of the clone of migrant founders to a new, already-existing ecological niche. It was established that monohostal specialization of the plague microbe was made possible due to heterothermia (5–37°C) of marmots in the hibernation period. The factors of the speciation process—isolation, the struggle for existence, and natural selection—were analyzed.     

Quantum Speciation of <Emphasis Type="Italic">Yersinia pestis</Emphasis> Plague Microbe in a Heteroimmune Environment: In the Populations of Hibernating Tarbagan Marmots (<Emphasis Type="Italic">Marmota sibirica</Emphasis>)

This review is devoted to the ecological mechanism for the transformation of the population of the psychrophilic saprozoobiont pseudotuberculosis microbe Yersinia pseudotuberculosis O:1b into the population of the obligate blood plague microbe Yersinia pestis in the host–parasite system of the marmot flea (Marmota sibirica–Oropsylla silantiewi). The correspondence of this mechanism to the evolutionary principle of quantum speciation has been shown. The most significant population–genetic microbial transformations took place in the populations of hibernating marmots. The main factor of rapid speciation was the heterothermic and, accordingly, heteroimmune state of host marmots during hibernation. During winter awakenings, the body temperature of marmots increases in an S-shaped manner from 5 to 37°C within a short period of time (from dozens of minutes to several hours). A drastic acceleration of metabolic and immune processes occurs in the temperature range of 20–30°C. Rapid adaptation to the “explosive” increase in the immune activity of the primary host (tarbagan marmot) during its regular winter awakenings was the essence of the process of Y. pestis speciation.     

Spheroplasts of plague microbe strains from the Transcaucasian uplands and their capacity for pesticin synthesis]

Spherical formations of the plague microbe strains from the Transcaucasian Upland, I plague microbe strain of the sandwort variety and I strain of the marmot variety were obtained under the effect of lithium chloride. They had the remains of the cell wall, were viable, sensitive to osmotic shock, preserved sensitivity to the specific bacteriophage and pesticins. All this was evident of isolation of the spheroplasts of the plague microbe. The spheroplasts showed a capacity for pesticin production. The pesticin synthesis by the spheroplasts of the plague causative agent from the Transcaucasian Upland increased with an increase in the content of lithium chloride in the medium. The largest inhibiiton zones were observed, when 0.7-0.8 per cent of lithium chloride were present in the medium. In the spheroplasts of the plague causative agent from the Mountain Altai (the marmot variety) the pesticin synthesis was inhibited with an increase in the content of lithium chloride in the medium. The activity spectrum of the pesticins of the spheroplasts of the plague causative agent from the Transcaucasian Upland and the spheroplasts of the strains of the marmot and sandwort varieties was broader than that of the rod-like forms of these strains. The indicator properties were found in the strains of the plague microbe of the marmot and sandwort varieties with respect to the pesticins of the spheroplasts of the sel-like producing organisms and organisms from the Transcaucasian Upland.     

The Multiple Faces of the Marmot: Associations with the Plague,Hunting, and Cosmology in Mongolia

Mongolians have long known of the association between marmots and the plague. We examine their understanding of the marmot not only as a biological species that can harbour the plague, but also from a cosmological perspective as a chimerical being with potential punishment on hunters who have transgressed ancient taboos. To do so we deconstruct the multiple image of the chimerical marmot in legends, stories, and beliefs. Many Mongolians believe that if the marmot is over-exploited and the population decimated through excessive hunting, hunting households may be punished with infections of the plague.

     

The influence of the host on the frequency of block formation in males and females of Citellophilus tesquorum altaicus Ioff, 1936 (Siphonaptera: Ceratophyllidae) and transmission of the plague pathogen by these fleas

Data obtained during feeding of infested females and males of Citellophilus tesquorum altaicus Ioff, 1936 (Siphonaptera: Ceratophyllidae), the main vector of plague in Tuva natural plague focus, on the natural hosts and on laboratory animals were analyzed. Sexual differences in fleas were found to depend on the host. Females fed more actively on longtailed ground squirrels Spermophilus undulatus than on white mice. The feeding activity of males on the two hosts did not differ. A higher mortality of infested females and males was observed during feeding on mice. The frequency of block formation and pathogen transmission in males was higher during bloodsucking on the ground squirrel; in females, during feeding on mice. Thus, sex-related differences in the plague pathogen transmission revealed in laboratory white mice may be not the same in nature. This should be taken into account when extrapolating the experimental data on the natural relations between the plague pathogen and ectoparasites.     

Genetic bases of methionine dependence in <Emphasis Type="Italic">Yersinia pestis</Emphasis> strains of main and non-main subspecies

Structural and functional organization of genes responsible for biosynthesis of amino acid methionine, which plays a leading role in cellular metabolism of bacteria, was studied in 24 natural Yersinia pestis strains of the major and non-main subspecies from various natural plague foci located in the territory of Russian Federation and neighbouring foreign countries, and also in Y. pestis and Y. pseudotuberculosis strains recorded in the files of NCBI GenBank database. Conservatism of genes metA, metC, metE, and metH as well as regulatory genes metR and metJ involved in biosynthesis of this amino acid was established. Sequencing of the variable locus of gene metB in natural Y. pestis strains of major and non-main subspecies revealed that the reason for the methionine dependence of strains belonging to the main subspecies is a deletion of a single nucleotide (−G) in the 988 position from the beginning of the gene, whereas this dependence in strains belonging to subspecies hissarica results from the appearance of a single nucleotide (+G) insertion in the 989 position of gene metB. These mutations are absent in strains of the caucasica, altaica, and ulegeica subspecies of the plague agent and in strains of pseudotuberculosis microbe, which correlates with their capacity for methionine biosynthesis.     

Yersinia pestis strains isolated in natural plague foci of Caucasus and Transcaucasia in the context of the global evolution of species

BackgroundPlague is a highly dangerous vector-borne infectious disease that has left a significant mark on history of humankind. There are 13 natural plague foci in the Caucasus, located on the territory of the Russian Federation, Azerbaijan, Armenia and Georgia. We performed whole-genome sequencing of Y. pestis strains, isolated in the natural foci of the Caucasus and Transcaucasia. Using the data of whole-genome SNP analysis and Bayesian phylogeny methods, we carried out an evolutionary-phylogeographic analysis of modern population of the plague pathogen in order to determine the phylogenetic relationships of Y. pestis strains from the Caucasus with the strains from other countries.ResultsWe used 345 Y. pestis genomes to construct a global evolutionary phylogenetic reconstruction of species based on whole-genome SNP analysis. The genomes of 16 isolates were sequenced in this study, the remaining 329 genomes were obtained from the GenBank database. Analysis of the core genome revealed 3315 SNPs that allow differentiation of strains. The evolutionary phylogeographic analysis showed that the studied Y. pestis strains belong to the genetic lineages 0.PE2, 2.MED0, and 2.MED1. It was shown that the Y. pestis strains isolated on the territory of the East Caucasian high-mountain, the Transcaucasian high-mountain and the Priaraksinsky low-mountain plague foci belong to the most ancient of all existing genetic lineages - 0.PE2.ConclusionsOn the basis of the whole-genome SNP analysis of 345 Y. pestis strains, we describe the modern population structure of the plague pathogen and specify the place of the strains isolated in the natural foci of the Caucasus and Transcaucasia in the structure of the global population of Y. pestis. As a result of the retrospective evolutionary-phylogeographic analysis of the current population of the pathogen, we determined the probable time frame of the divergence of the genetic lineages of Y. pestis, as well as suggested the possible paths of the historical spread of the plague pathogen.     

Habitat preferences in gray marmots (Marmota baibacina)

We examined habitat preferences of the Southern Altai subspecies of gray marmots (Marmota baibacina baibacina) both at the small and large scale. Considerable differences in habitat use among the gray marmot (sub)species complex have been described; Marmota kastschenkoi possibly represents the only forest-dwelling Palearctic marmot. Our results show that habitat use in Southern Altai marmots is determined mainly by vegetation type. The Altai marmots preferred grasslands and shrublands and their distribution was limited to the alpine zone above timberline. Marmots clearly avoided woodlands, even the forest edges and forest-steppe areas with a tree cover greater than 10 %. Gray marmots occur rarely in habitats occupied by alpine pikas, whereas presence of ground squirrels had no effect on marmot distribution. Altai marmots preferred mesic habitats with permeable subsoil layers. Livestock grazing and human disturbance did not affect marmot occurrence. Habitat requirements of examined Altai subspecies M. baibacina baibacina differ from the forest-steppe M. kastschenkoi; nevertheless, the ecological factors to which the forest-dwelling species responds remain to be analyzed. A recent speciation process in gray marmot complex was followed by the evolution of ecological requirements resulting in adaptation to forest dwelling.     

A review of flying fishes of the subgenus Hirundichthys (genus Hirundichthys, exocoetidae). 1. Oceanic species: H. speculiger, H. indicus sp. nova

A systematic revision of flying fishes of the subgenus Hirundichthys s.str was carried out based on a study of meristic and morphometric traits and characteristics of pigmentation of fishes from the local populations of species belonging to the subgenus. It is found out that the subgenus includes four species: oceanic H. speculiger from the Atlantic, Pacific and Indian Oceans, oceanic H. indicus sp.n. from the waters of the Indian Ocean, nerito-oceanic H. oxycephalus from the waters of the Indo-West Pacific and nerito-oceanic H. affinis from the Atlantic Ocean. The first part of the review focuses on two oceanic species with a large “mirror” on the pectoral fins: H. speculiger and H. indicus. A comparison of local populations showed that the species H. indicus is polytypic and consists of two subspecies. One of the subspecies—nominative H. indicus indicus—is distributed in the western and the central parts of the Indian Ocean and the other—H. indicus orientalis ssp.n.—in the Eastern Indian Ocean. Maps showing a geographical distribution of the species and the subspecies in the World Ocean are drawn up.     

Notes on the fleas Xenopsylla vexabilis Jordan, 1925 (Pulicidae: Siphonaptera) in Vietnam as related to the problem of anthropogenic plague foci

In the first half of the XX century, the flea Xenopsylla vexabilis, the main vector of the plague agent in the “natural plague foci” of the Hawaii, was shown to be a specific parasite of the small white-toothed rat Berylmys berdmorei, inhabiting the tropical forests and grasslands of Indochina, including Vietnam. X. vexabilis was not recorded in Vietnamese settlements. This flea was found in the fields bordering natural landscapes and agricultural areas as a parasite of the greater bandicoot rat Bandicota indica, Savile’s bandicoot rat B. savilei, and the rat Rattus koratensis. It was assumed that bandicoot rats may have played an important role in the introduction of the flea to the Pacific islands where X. vexabilis was then established on synanthropic rats. The new data do not support the concept of coevolution of the recent epizootic association Rattus exulans-Xenopsylla vexabilis-Yersinia pestis.     

Origin of the plague microbe <Emphasis Type="Italic">Yersinia pestis</Emphasis>: Structure of the process of speciation

The origin and evolution of the plague microbe Yersinia pestis are considered in the context of propositions of modern Darwinism. It was shown that the plague pathogen diverged from the pseudotuberculous microbe Yersinia pseudotuberculosis O:1b in the mountain steppe landscapes of Central Asia in the Sartan: 22000-15000 years ago. Speciation occurred in the tarbagan (Marmota sibirica)-flea (Oropsylla silantiewi) parasitic system. The structure of the speciation process included six stages: isolation, genetic drift, enhancement of intrapopulational polymorphism, the beginning of pesticin synthesis (genetic conflict and emergence of hiatus), specialization (stabilization of characteristics), and adaptive irradiation (transformation of the monotypic species Y. pestis tarbagani into a polytypic species). The scenario opens up wide prospects for construction of the molecular phylogeny of the plague microbe Y. pestis and for investigation of the biochemical and molecular-genetic aspects of “Darwinian” evolution of pathogens from many other nature-focal infections.     

Ecological Aspects of Evolution of the Plague Microbe Yersinia pestis and the Genesis of Natural Foci

A new hypothesis of the origin of the plague microbe in the Mongolian bobak (Marmota sibirica Radde, 1862) populations in Central Asia during the Pleistocene is based on the ideas of its relative phylogenetic recency. The Late Pleistocene cooling, which induced a deep freezing of the grounds in southern Siberia, Mongolia, and Manchuria, is considered as an inducer of speciation. The main ecological factors of the plague microbe evolution include the species specific behavior of the Mongolian bobak as it prepared to hibernate related to its occurrence in arid petrophytic landscapes and the larval parasitism of the flea Oropsylla silantiewi Wagn., 1898 in winter. Genesis of the plague foci is divided into two periods: natural-historical and biosocial. During the first period, the primary natural foci in Eurasia were formed and, during the second period, synanthropic (rat) and secondary natural foci appeared with the participation of humans in Africa, The New World, and on some tropical islands.     

Disentangling the Population Structure and Evolution of the Clam Pathogen Vibrio tapetis

Vibrio tapetis is a fastidious slow-growing microorganism that causes the Brown Ring Disease in clams. Recently, two subspecies for this bacterial pathogen have been proposed. We have developed a multilocus sequence typing scheme and performed evolutionary studies of V. tapetis population using the great majority of isolates of V. tapetis obtained worldwide until now (30 isolates). V. tapetis constitutes a high polymorphic population, showing low diversity indexes and some genetic discontinuity among the isolates. Mutation events are more frequent than recombination, although both are approximately equally important for genetic diversification. In fact, the divergence between subspecies occurred exclusively by mutation but the diversity observed among isolates of the same subspecies appeared to be generated mostly by recombination. Between the subspecies, genetic distance is very high and almost no recurrent gene flow exists. This pathogen displays a non-clonal population structure with an ancient spatial segregation population and some degree of geographical isolation, followed by a population expansion, at least for V. tapetis subsp. tapetis. A database from this study was created and hosted on publmlst.org (http://pubmlst.org/vtapetis/).     

Defensive behaviour and its inheritance in the anabantoid fish, Macropodus opercularis and Macropodus opercularis concolor

In this preliminary study defense behaviour patterns (fear responses) are described in two closely related, behaviourally different inbred labyrinth fish subspecies and in their F₁ generation. The subspecies M. opercularis (characterized briefly by “active escape”) and M. opercularis concolor (characterized by “passive escape”) showed specific differences in the manifestation of certain defense behaviour patterns. In the F₁ hybrid generation dominance and overdominance of M. opercularis was found in most defense behaviour patterns. Analysing the frequencies and sequences of movement patterns it could be shown that defensive behaviour is not a random or entirely “plastic” process but that there is sequential linkage between the patterns and they form characteristic clusters. Our results suggest that manifestations of different patterns are under genetic control and presumably, genetic determination of certain patterns is not very complex. Attempts were made to determine whole brain noradrenaline, serotonine and dopamine levels of the two subspecies and a significant difference was found in the noradrenaline content.     

Progress in the 21st century: a Roadmap for the Ecological Society of Japan

The primary goal of the 60th anniversary symposium of the Ecological Society of Japan (ESJ) was to re-examine the role of the Society. The first of five lectures, “Development of Long-term Ecological Research in Japan,” discussed the increasingly important role of long-term and networked research studies. Ecological research in Asia faces many challenges, because Asia features natural and anthropogenic landscapes with highly diverse ecosystems. “Developing Strategies of the Ecological Society of Japan for Worldwide Societies of Ecology with Special Reference to Strategies for Asia” emphasized the role of ESJ in promoting ecological research and outreach in Asia. Ecosystem sustainability is a key issue in both the theory and practice of ecosystem management. A framework concept of an environmental and biodiversity cycle was proposed in the session “Linking Community and Ecosystem Dynamics” for understanding the mechanisms driving the sustainability of ecosystems. Ecosystem services are essential aspects of land use and conservation planning and management. “Integrating Models of Ecosystem Services and Land Use Changes” reviewed recently-developed models that simulate patterns of land-use change and analyze its effects on ecosystem services and also recommended future directions for collaboration among researchers. “Disaster Resilience and Coastal Ecology” highlighted the contributions of ecologists to evaluating the resilience of damaged coastal ecosystems and provided sound proposals to local communities and governments for rehabilitation plans. The past achievements and future directions of ESJ were discussed by the panelists and the audience in “Past and Future of the Ecological Society of Japan.”     

Genetic bases of methionine dependence in Yersinia pestis strains of major and non-major subspecies

Structural and functional organization of genes responsible for biosynthesis of amino acid methionine, which plays a leading role in cellular metabolism of bacteria, was studied in 24 natural Yersinia pestis strains of the major and minor subspecies from various natural plague foci located in the territory of Russian Federation and neighbouring foreign countries, and also in Y. pestis and Y. pseudotuberculosis strains recorded in the files of NCBI GenBank database. Conservatism of genes metA, metB, metC, metE, and metH as well as regulatory genes metR and metJ involved in biosynthesis of this amino acid was established. Sequencing of the variable locus of gene metB in natural Y. pestis strains of major and minor subspecies revealed that the reason for the methionine dependence of strains belonging to the major subspecies is a deletion of a single nucleotide (-G) in the 988 position from the beginning of the gene, whereas this dependence in strains belonging to subspecies hissarica results from the appearance of a single nucleotide (+G) insertion in the 989 position of gene metB. These mutations are absent in strains of the caucasica, altaica, and ulegeica subspecies of the plague agent and in strains of pseudotuberculosis microbe, which correlates with their capacity for methionine biosynthesis.     

Special Issue Oceans and Humans Health: The Ecology of Marine Opportunists

Opportunistic marine pathogens, like opportunistic terrestrial pathogens, are ubiquitous in the environment (waters, sediments, and organisms) and only cause disease in immune-compromised or stressed hosts. In this review, we discuss four host–pathogen interactions within the marine environment that are typically considered opportunistic: sea fan coral–fungus, eelgrass–Labyrinthula zosterae, sea fan–Labyrinthulomycetes, and hard clam–Quahog Parasite Unknown with particular focus on disease ecology, parasite pathology, host response, and known associated environmental conditions. Disease is a natural part of all ecosystems; however, in some cases, a shift in the balance between the host, pathogen, and the environment may lead to epizootics in natural or cultured populations. In marine systems, host–microbe interactions are less understood than their terrestrial counterparts. The biological and physical changes to the world’s oceans, coupled with other anthropogenic influences, will likely lead to more opportunistic diseases in the marine environment.     

Components of the major urinary protein complex of inbred mice: Determination of NH2-terminal sequences and comparison with homologous components from wild mice

The major urinary protein (MUP) complex of normal inbred laboratory mice (Mus musculus musculus) is a family of three electrophoretically distinguishable components, designated 1, 2, and 3 in order of increasing anodal mobility at pH 5.5. Components 1 and 2 are under the control of a single genetic locus; the MUP complex of a given inbred strain consists of component 1 or 2 plus component 3. In this study, the urinary protein of two subspecies of Asian wild mice, Mus musculus molossinus (originally trapped in Japan) and Mus musculus castaneus (originally trapped in Thailand), was examined electrophoretically and ultracentrifugally. The MUP complex of male M. m. molossinus and M. m. castaneus sedimented at approximately the same rate as that of M. m. musculus (s ₂₀ =2.0?2.2S). It consisted of a “fast” (i.e., more anodal than component 3) and an “intermediate” component plus one or more “origin” (i.e., less anodal than component 1) components. The “fast” and “origin” components were isolated chromatographically, and NH₂-terminal sequences spanning the first 36 residues were determined. Comparison with the NH₂-terminal sequences determined for components 1, 2, and 3 isolated from the urine of BALB/c or C57BL/6 mice revealed, except for a single replacement at position 6 in the “origin” component of M. m. molossinus, no differences among the 1, 2, “origin”, and “fast” components. Component 3 was highly homologous but differed from component 1 at nine positions; its residue at position 6 was the same as that of the M. m. molossinus “origin” component.     

Needle terpene concentrations and emissions of two coexisting subspecies of Scots pine attacked by the pine processionary moth (Thaumetopoea pityocampa)

Mediterranean pine forests are often attacked by caterpillars of Thaumetopoea pityocampa (Lep., Thaumetopoidae), one of the most important defoliators in the Mediterranean region causing large economic losses and ecological effects. The needle terpene concentrations and emissions may play a key role in the defense of pines. We studied two subspecies of Pinus sylvestris, nevadensis (an endemic and relict subspecies) and iberica , with different levels of caterpillar attack in Sierra Nevada mountains (Spain). GC–MS analyses showed large total concentrations of terpenes (6 to 39 mg g^?1 of dry weight) in the needles of both subspecies under field conditions. Concentrations were 25 % higher in “Non-Attacked Trees” (NATs) of the iberica than in the nevadensis subspecies. The branches of NATs had terpene concentrations 20 % higher than those of “Attacked Branches of attacked trees” (ABs). Within attacked trees, the “Non-Attacked Branches” (NABs) also had terpene concentrations 20 % higher than those of ABs. Mainly α-pinene and germacrene D had higher concentrations in NATs and NABs than in ABs. Some terpenes had higher concentrations in NABs than in NATs, indicating possible systemic reactions. In subsp. nevadensis, the percentage of monoterpenes relative to total terpenes was higher in ABs than in other attack states. The rates of emission in nevadensis (standardized to 30 °C) were ca. three times higher in ABs than in NABs and NATs. These results suggest that the lower terpene concentrations and high percentages of monoterpenes in ABs were produced by a combination of emission losses and terpene induction in response to herbivorous attack.