S32 REVISÃO REVIEW Environment, interactions between Trypanosoma cruzi and its host, and health Meio-ambiente, interações entre Trypanosoma cruzi e seu hospedeiro e saúde humana Antonio R. L. Teixeira 1 Clever Gomes 1 Silene P. Lozzi 1 Mariana M. Hecht 1 Ana de Cássia Rosa 1 Pedro S. Monteiro 1 Ana Carolina Bussacos 1 Nadjar Nitz 1 Concepta McManus 1 Abstract The ancient game 1 Faculdade de Medicina, An epidemiological chain involving Trypanoso- To understand the relationships amongst liv- Universidade de Brasília, Brasília, Brasil. ma cruzi is discussed at the environmental level, ing organisms with extensive epidemiological and in terms of fine molecular interactions in chains, affecting both health and species surviv- Correspondence invertebrate and vertebrate hosts dwelling in dif- al, requires that we begin when life began, in salt A. R. L. Teixeira 1,2 Laboratório Multidisciplinar ferent ecosystems. This protozoan has a complex, water . During the early Proterozoic era (the de Pesquisa em Doenças genetically controlled plasticity, which confers pre-Cambrian period) approximately 4.5 billion de Chagas, Faculdade de adaptation to approximately 40 blood-sucking years ago, primitive life forms such as eubacte- Medicina, Universidade de Brasília. triatomine species and to over 1,000 mammalian ria and archeabacteria emerged from the organic C. P. 04536, Brasília, DF species, fulfilling diverse metabolic requirements soup on the earth’s crust. These pro-karion mi- 70919-970, Brazil. in its complex life-cycle. The Tr. cruzi infections croorganisms incorporated organic constituents [email protected] are deeply embedded in countless ecotypes, where (proteins, nucleic acids, lipids and carbohy- they are difficult to defeat using the control meth- drates) which gave rise to life. In the presence of ods that are currently available. Many more field these ingredients, microorganisms initiated the and laboratory studies are required to obtain data synthesis of ATP (adenosine-triphosphate), uni- and information that may be used for the control versally used for energy storage 2,3. and prevention of Tr. cruzi infections and their Every miniscule organism on earth may come various disease manifestations. Emphasis should in to contact with every other, given sufficient be placed on those sensitive interactions at cellu- time 4. This “game” resulted in a revolution ap- lar and environmental levels that could become proximately 1.5 billion years ago. The approxi- selected targets for disease prevention. In the mation of archea and eubacteria led eventually short term, new technologies for social mobiliza- to their association. Subsequently, a biochemi- tion should be used by people and organizations cal event probably determined cooperation and working for justice and equality through health exchange of nutrients among these organisms. information and promotion. A mass media di- Extreme solidarity became symbiosis, resulting rected program could deliver education, informa- in the formation of undulipodia. This ancient tion and communication to protect the inhabit- protozoan retained its flagellum, which emerged ants at risk of contracting Tr. cruzi infections. from the mitochondrion of an archea bacteria spirochete. Other organelles from eubacteria Trypanosoma cruzi; Chagas Disease; Host-Para- completed the biochemical machinery of this eu- site Interactions; Environment karion, a unicellular living microorganism which Cad. Saúde Pública, Rio de Janeiro, 25 Sup 1:S32-S44, 2009 ENVIRONMENT, INTERACTIONS BETWEEN Tr. cruzi AND ITS HOST, AND HEALTH S33 contained membrane-wrapped DNA, in a pack- ment and a constant change in the temperature. age-type nucleus. In this environment macroscopic plants grew, At present, morphological evidence at the ul- with roots for uptake from soils and vascular sys- tra structural and molecular levels are consistent tems for distribution through the plant; in turn, with this pathway of primitive life 2. these plants became a major source of food for An occurrence 670 million years ago resulted animals. Those changes made grounds for co- in ancestral eu-karion undulipodia giving rise to evolution of Annelida-Molusca, which are close primitive trypanosomes, which were promptly relatives of Arthropods, and of vascular plants. recognized in fish. The flagellate protozoa Try- Paleontological data indicate that the invasion panosoma gray, which occurs in crocodiles, of the terrestrial environment by vascular plants, is related to mammal trypanosomes 5. It was, arthropods and higher vertebrates occurred rela- therefore, assumed that reptiles and batrachi- tively late, after the invertebrate phyla were well ans were primitive vehicles that brought these established in marine environments. Among the flagellates onto solid ground. The presence of vascular plants, the pteridophytes relied upon trypanosomatids in the blood of aquatic inverte- spores for dispersal. Among animals, complete brates and vertebrates favored secondary acqui- adaptation to plant-sucking resulted from the sition of whole microorganisms by a host during development of mouth-parts with a pump con- the Phanerozoic period, 570 million years ago 4. nected to the proboscis 5. Experiments using pte- These interactions among the trypanosomes and ridophytes and living arthropods indicate that cold-blooded animals require further study. The some spores remain viable after passing through construction and remodeling of the undulipodia the gut and hence it is believed that this feeding served to fabricate metazoans. These occurrenc- habit may have also been advantageous to some es explain multicellular organization, which de- early plants for propagule dispersion 6. It has pends on relationships at molecular and physi- been proposed that many occurrences provided ological levels. The concepts in this review paper the grounds for diversification into over a mil- show that life is a continuous process and con- lion species of arthropods in the Class Insecta: stantly changing. Hemiptera that presently inhabit the earth 7. This The protozoa that belong to the Class Zoo- reasoning can help to explain the happenings mastigophorea (Eukaryota, Excavata, Eugleno- during the Devonian epoch, 360 million years zoa) include the Kinetoplastid flagellates of the ago, where accounts of wide scale exchange of Trypanosomatidae family and have a major im- organelles, messengers and moieties have been pact on public health and veterinarian medicine. reported among early species of life 2,8. Numer- Phylogenetic analyses have placed the protozoan ous representatives of the Class Insecta may have Tr. gray, that can be found in the blood of croc- become second stage vehicles for the delivery of odiles and possibly date to around 480 million macromolecules which were widely exchanged years ago, at the root of the kinetoplastids, next between species. It appears that these insects to bodonids (Bodo saltans). These kinetoplastids became dependent on vascular plant carbohy- include Tr. cruzi, the agent of Chagas disease in drates that were sucked in by its mouth parts, the Americas, Tr. brucei, the agent responsible for leading to the accumulation of large energy sur- sleeping sickness in Africa, and the Leishmania pluses. These surpluses could be readily used for species that infect mammals and produce differ- subsequent transportation and delivery of whole ent forms of diseases worldwide 3. The life-cycles microorganisms or their spare-parts during fur- of these trypanosomatids account for their major ther interactions with newcomers. division into Salivarian and Stercorarian branch- es, completing the infective metacyclic stages, respectively, in the salivary gland and in the hind Efficient oxygen transportation system gut of invertebrate vectors. This feature intro- in warm-blooded animals duces important diversifications in the mode of infection transmission to mammals. During early life, the plant and animal kingdoms branched into two different energy-producing systems. Photosynthetic chloroplasts in green Vascular plants and the emergence of plants captured energy directly from the solar invertebrate-vectors system, and mitochondrion cytochrome in ex- tant microorganisms used anaerobic metabo- During the Paleozoic and Silurian periods, around lism which enabled them to survive during a time 434 million years ago, drastic changes in the mix- when oxygen on the earth’s surface was scarce ture of atmospheric gases led to an increase in 2,8. Following modifications in the gas composi- the oxygen diffusion coefficient in the environ- tion of the atmosphere, a respiratory chain de- Cad. Saúde Pública, Rio de Janeiro, 25 Sup 1:S32-S44, 2009 S34 Teixeira ARL et al. veloped in vertebrate animals that carry ionized reptiles were ancient reservoirs of Tr. cruzi pop- Fe2+ in the hemoglobin molecule. A constant ulations, now infecting man and domesticated flux of hemoglobin-rich red blood cells made mammals. Some insects deciphered that hema- it possible for hemin-bound Fe2+ to become an tophagy helped their development and growth, important link in a metabolic pathway which hence small animals that populated the Ameri- is closely related to species fertility and repro- can Continent became providers of blood for duction 9,10. In vertebrate animals, an increase these predators. in oxygen led to complex biochemical pathways Triatomine and Tr. cruzi coevolution is gener- using a high consumption of glucose and energy ally considered to have been amazingly success- production, resulting from