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Modelling the Transport of Nutrients in Early Animals

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Modelling the Transport of Nutrients in Early Animals Evol Biol (2009) 36:256–266 DOI 10.1007/s11692-008-9047-2 ESSAY Modelling the Transport of Nutrients in Early Animals N. J. Beaumont Received: 20 June 2008 / Accepted: 6 November 2008 / Published online: 10 January 2009 Ó Springer Science+Business Media, LLC 2008 Abstract The single-celled ancestors of multi-cellular Introduction animals (metazoans) did not need to transport nutrients between cells, but this ability is vital for modern animals. The origins of multi-cellularity are obscure. It is unclear How could intercellular nutrient transport have begun? how early multi-cellular animals evolved, and why it And how did this influence the early evolution of animals? happened at that particular time. Suggestions or hypotheses In this hypothesis, I suggest that nutrients could have about the origins can be tested using the main lines of passed directly between the cytoplasm of conjoined cells in available evidence about the earliest animals: the fossil early compacted cell-balls, along the plane of the closed record and the molecular and developmental data from epithelium. This would have limited early animals to the modern species. size and form of modern embryos. The mechanisms that The Precambrian fossil record provides evidence of the indirectly transport nutrients between discrete cells, via the earliest known multi-cellular forms. Multi-cellular organ- extracellular fluid within the body-space, are modelled to isms have been identified from rocks up to 600 million years have evolved sequentially; so comparison of nutrient old. A diverse group of large fossils, the Ediacaran Fauna, transport processes could provide evidence of any early have been found at sites around the World in rocks from divergences of phyla. When the last of the indirect inter- between approximately 580 million and 550 million years cellular transport processes for essential nutrients had been ago. It has been suggested that these frondose organisms developed, the extracellular fluid within the body-space were ancestral to some modern animals (Glaessner and would have contained all necessary nutrients. Then the Wade 1966). However, an alternative hypothesis has been epithelium could have greatly expanded, and cells lived suggested: that they were an independent ‘‘experiment’’ in and divided within the body-space. This development of multi-cellularity (Seilacher 1984). At this stage, it is unclear nutrient transport processes would have enabled animals to whether these organisms were ancestral to modern phyla. greatly increase in size and complexity. Microfossils have been found in southern China from approximately 580 million years ago (Xiao et al. 1998; Keywords Metazoan Evolution Cambrian Chen et al. 2000). These minute fossils are less than a Proterozoic Á Á Á millimetre across but are exquisitely preserved. They have been interpreted as embryonic forms; but the adult forms do not seem to be present—so it is unclear how they should be incorporated into an account of early multi-cellularity. A putative bilaterian from this area has also been reported. Vernanimalcula (Chen et al. 2004a) has been interpreted as N. J. Beaumont (&) having a mouth, gut and anus in a hollow form of less than Department of Medicine, Royal Free & University College a millimetre; however this interpretation is controversial Medical School, Royal Free Campus, Rowland Hill Street, (Bengtson and Budd 2004; Chen et al. 2004b). London NW3 2PF, UK e-mail: [email protected]; Animals from extant phyla definitely start to appear in [email protected] the fossil record from around 530 million years ago. The 123 Evol Biol (2009) 36:256–266 257 apparently sudden appearance of a broad range of complex in the fossil record. Nevertheless, it is clear that multi- animals from virtually all recognised phyla has been called cellular creatures arose from simpler organisms, as surely the Cambrian ‘‘explosion’’. Taking the fossil record on its as the adult develops from the fertilized egg by way of the own, it suggests that animals with bodyplans similar to embryo, so it is intriguing to consider the reasons and modern animals appeared suddenly, with no obviously requirements for such changes. simpler precursors. There is continuing debate over whe- The aim here is to understand the advent of multi-cel- ther this is an artefact of the fossil record or an accurate, if lularity by considering how nutrients move between the rather puzzling, record of events. cells of modern animals, and then considering how this The comparison of homologous molecular sequences distribution could have begun. I argue that these processes from different modern phyla, calibrated with reference to would not have developed in unicellular organisms, but the fossil record, has been used to create ‘‘molecular that they are necessary for triploblastic metazoans. I pres- clocks’’. These data have been used to extrapolate back to ent a model of early nutrient transport in animals, suggest the metazoan radiation, to estimate the time when the stem how this may have evolved into modern forms and con- groups that led to modern phyla diverged. In contrast to the sider some of the implications this had for evolution. impression formed from the fossil record, many of the studies based upon molecular data have suggested that The Transport of Nutrients in Animals modern phyla diverged a long time before the Cambrian period (Wray et al. 1996; Pisani et al. 2004). These studies The cells of multi-cellular organisms must obtain sufficient suggest that the ancestral stem groups of modern phyla had nutrients from either the environment or from within the diverged for a considerable length of Precambrian time organism. Nutrients pass between cells in triploblastic without leaving traces in the fossil record. This is surpris- animals by a variety of methods. These processes can be ing because the stem groups of modern phyla were divided into direct and indirect transport, depending upon probably multi-cellular. However, there may have been a whether the molecules that are being transported pass number of gene, and even genome, duplications around the across cell membranes and through another compartment time of the metazoan radiation, and rates of genetic change when moving between cells. In direct transport, nutrients could have varied between phyla. These factors may have pass between cells via cytoplasmic bridges (such as gap jeopardized the assumption of uniform rates of variation junctions). These link the cytoplasm of conjoined cells and upon which this approach is based (Peterson et al. 2004). allow small molecules to non-specifically equilibrate It is difficult to understand the beginning of multi-cel- between them without having to cross extracellular space lular animals because it is unclear how the metazoan or the plasma membrane (Fig. 1a). This can happen in cell- radiation, when the variety of modern phyla first arose— types such as epithelia or syncitia. which has been investigated by analyzing molecular However, there are some cell types, such as muscle, sequences, was related to the Cambrian ‘‘explosion’’ seen bone and blood cells, which are not conjoined with other AB Fig. 1 Nutrients can pass between cells by direct or indirect Nutrients are released into the enclosed body-space by the cells that nutrient transport. Simplified representation in which only two take them up from the gut. They are then available for other cells nutrients (blue and red) are depicted in cross-sections of hypothetical (such as the token isolated internal cell depicted). Note that a separate gastrula-like forms. a Direct nutrient transport: Both nutrients are indirect nutrient transport process is required for each nutrient. taken up into the organism and pass from cell to cell by cytoplasmic Nutrients are only depicted in the top half of the figure links across the closed epithelium. b Indirect nutrient transport: 123 258 Evol Biol (2009) 36:256–266 cells and take up all the nutrients they require from the Therefore, metazoan nutrient uptake processes could have extracellular fluid. This requires that they have all the derived from those used by unicellular organisms. necessary transport mechanisms to take up each nutrient as needed across the plasma membrane, and also that all Nutrients Could have Moved Between Cells Within essential nutrients are present in the extracellular fluid. Early Animals by Direct Transport This in turn requires that the cells that take up the nutrients from food (for example, the enterocytes that line the Some cells in early multi-cellular organisms would have mammalian gut) also release these nutrients into the needed to receive nutrients from other cells when their extracellular space within the organism so that they may be ability to take up nutrients from the environment became taken up by other cells. This mode of intercellular nutrient limited because their access to food was hampered by their transport is here designated indirect, to denote that the position in the organism. This movement of nutrients could nutrients pass between cells by crossing the plasma mem- have happened by direct transport. Cytoplasmic bridges brane, moving across the extracellular space within the would have established a physical link between cells, organism and then crossing the membrane of another cell which would have coupled the pools of solutes in them (Fig. 1b). without requiring the development of specialized transport The two processes that move nutrients between the cells processes for each nutrient. This ability
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