Uni-cellular integration of complex spatial information in slime moulds and ciliates

https://doi.org/10.1016/j.gde.2019.06.012Get rights and content

Single-celled organisms show a fascinating faculty for integrating spatial information and adapting their behaviour accordingly. As such they are of potential interest for elucidating fundamental mechanisms of developmental biology. In this mini-review we highlight current research on two organisms, the true slime mould Physarum polycephalum and the ciliates Paramecium and Tetrahymena. For each of these, we present a case study how applying physical principles to explain behaviour can lead to the understanding of general principles possibly relevant to developmental biology.

Introduction

When we think of development, we usually mean the process of creating an organised, multi-cellular organism out of a single cell. From each cell's point of view, however, the problem is simply how to integrate different signals indicative of its own spatial situation that determine behaviour, shape, and differentiation.

The basic cell structure is conserved throughout eukaryotes, at least as regards their composition of organelles (the nucleus, mitochondria, the endoplasmic reticulum, the Golgi apparatus, etc.), although there are exceptions (the cell wall, chloroplasts). Many aspects of the cell's molecular machinery, too, are commonly shared amongst very diverse clades of life (e.g., DNA replication, signalling pathways, etc.). Due to this structural and mechanistic conservation, it may be reasonable to expect homologies in how cells work in time and behave, both independently and collectively, in response to external stimuli.

We emphasise two major methods of cell movement: First, amoeboid crawling is reduced to the common basic processes of actin filament polymerisation and pseudopod formation. Second, speed and direction of ciliated swimming is reduced to the periodic beating of individual cilia and their spatio-temporal synchronisation.

Thus, it may be rewarding to study single-celled organisms that show a fascinating faculty for integrating spatial information and adapting their behaviour accordingly. Then we may ask what physical models we can find that generalise the organisms’ ability and apply them to larger ranges of organisms [1].

Below, we will introduce research following the above approach focussing on two important model organisms. One is an example for amoeboid locomotion, the other is a ciliate. For each, we will discuss a case study and an overview of recent research in the field.

Section snippets

Cellular cognition in a unicellular slime mould

The unicellular slime mould Physarum polycephalum is of particular interest for studies of cellular cognition, because it is easy to handle and macroscopic, with a single cell easily spanning several 100 cm2; and because it has been enjoying research from many different angles that provide a rich background of cross-disciplinary results [2,3].

Integration of spatial information in ciliates

In addition to the adherent locomotion, swimming is one of the important ways to migrate for unicellular microorganisms. Ciliates, a kind of eukaryotic microorganisms which play important roles in the earth's environments [41], exhibit a rapid swimming motion. The cellular surface of ciliates is covered in a large number of hair-like organelles, termed cilia, the beating of which propels the cells through water. Some ciliates adapt their behaviour according to the geometry of their surroundings

Conclusion

The fundamental units of all living things are cells. This statement has two important consequences [1]. It means, first, that ‘below’ the level of the cell, at the level of its components, we are confronted with the realm of physical interactions and chemical reactions. The second meaning is that we can expect commonalities in the mechanisms governing very diverse behaviours in vastly different organisms based on their common unit of organisation, the cell.

During development, individual cells

Acknowledgements

This work was performed under the Cooperative Research Program of "Network Joint Research Center for Materials and Devices" (T.N.,K.S.,Y.N.). This work was supported by the JSPS KAKENHI Grant No. 17H02939 and 18H01135 (K. S.), and by the JSPS Core-to-Core Program, A. Advanced Research Networks, as well as by the NIBB Collaborative Research Program to 19-505 (Y.N.) and the the Program for Fostering Researchers for the Next Generation conducted by Consortium Office for Fostering of Researchers in

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