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Acidocalcisomes ? conserved from bacteria to man

Abstract

Recent work has shown that acidocalcisomes, which are electron-dense acidic organelles rich in calcium and polyphosphate, are the only organelles that have been conserved during evolution from prokaryotes to eukaryotes. Acidocalcisomes were first described in trypanosomatids and have been characterized in most detail in these species. Acidocalcisomes have been linked with several functions, including storage of cations and phosphorus, polyphosphate metabolism, calcium homeostasis, maintenance of intracellular pH homeostasis and osmoregulation. Here, we review acidocalcisome ultrastructure, composition and function in different trypanosomatids and other organisms.

Key Points

  • Acidocalcisomes are acidic and dense organelles ? both by weight and by electron microscopy ? with a high concentration of phosphorus present as pyrophosphate and polyphosphate (poly P) that is complexed with calcium, and other elements.

  • Acidocalcisomes are related to organelles previously named volutin or metachromatic granules, and polyphosphate vacuoles, which were thought to function as storage granules.

  • The acidocalcisome membrane can contain several pumps (Ca2+-ATPase, V-H+-ATPase, V-H+-PPase), exchangers (Na+/H+, Ca2+/H+), and channels (aquaporins), while its matrix contains enzymes related to pyrophosphate and polyphosphate metabolism (exopolyphosphatase, polyphosphate kinase, pyrophosphatase).

  • After their identification in trypanosomatids, acidocalcisomes were found in other microorganisms such as Toxoplasma gondii, Plasmodium spp., the green alga Chlamydomonas reinhardtii, and the slime mould Dictyostelium discoideum. The recent identification of acidocalcisomes in bacteria (Agrobacterium tumefaciens, Rhodospirillum rubrum) and the finding that human platelet dense granules are homologous to acidocalcisomes, indicates that these organelles have been conserved during evolution from bacteria to humans.

  • Acidocalcisomes have been linked with several functions, including storage of cations and phosphorus, polyphosphate metabolism, calcium homeostasis, maintenance of intracellular pH homeostasis, and osmoregulation. This review describes acidocalcisome ultrastructure, composition and function in different trypanosomatids with an overview of our knowledge of the organelle in other organisms.

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Figure 1: Schematic representation of trypanosomatids.
Figure 2: Thin sections of acidocalcisomes of trypanosomatid parasites prepared by different transmission electron microscopy methods and of hydrogenosomes of Tritrichomonas foetus.
Figure 3: Morphology of acidocalcisomes in whole trypanosomatids.
Figure 4: Schematic representation of a typical acidocalcisome.

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Acknowledgements

Work in our laboratories was funded by the US National Institutes of Health (to R.D. and S.N.J.M.), the Burroughs Wellcome Fund (to R.D. and S.N.J.M.) and Programa de Núcleos de Excelência (to W.S.).

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Correspondence to Roberto Docampo.

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DATABASES

Entrez

Agrobacterium tumefaciens

Chlamydomonas reinhardtii

Dictyostelium discoideum

Plasmodium falciparum

Rhodospirillum rubrum

SwissProt

TbKIFC1

FURTHER INFORMATION

Roberto Docampo and Silvia Moreno's laboratories

Glossary

AXONEME

A cytoskeletal structure of microtubules that forms flagella and cilia.

CYTOSTOME

An invagination of the plasma membrane that is used to incorporate external material.

MORPHOMETRIC STUDY

The diameter of acidocalcisomes in electron microscopy sections is measured and their volume is calculated assuming that they are perfect spheres.

DIGENETIC TRYPANOSOMATIDS

Trypanosomes that have two hosts, in contrast to monogenetic trypanosomatids which only have one host.

SPONGIOME

Tubules and vacuoles that are connected to the contractile vacuole.

PULSATION PERIOD

The period of time between contractions of the contractile vacuole.

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Docampo, R., de Souza, W., Miranda, K. et al. Acidocalcisomes ? conserved from bacteria to man. Nat Rev Microbiol 3, 251–261 (2005). https://doi.org/10.1038/nrmicro1097

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