Sponge sneeze: sensing and contracting

By Daniella Dawson Rastelli (Pitzer College) and Dylan Morris (Pitzer College) [Edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only.]

Sponge contractions, why it matters:

Porifera are one of the most basal of metazoan phyla, they lack nerves and muscles but nonetheless are capable of responding to changes in their environment. Ludeman et al. (2014) discuss a novel find in sensory evolution in their paper “Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges”. Most metazoans use cilia as sensory appendages (“antennae”) and in cell-to-cell signaling. Although commonly found in larval stages of the poriferan lifecycle, the presence of non-motile cilia in mature sponges may provide insight into the evolution of complex sensory structures involving cilia present in more derived metazoans.

What did they do?

The authors demonstrated that non-motile cilia present in the water-flow regulating structure, the osculum, are involved in flow-sensation and coordinated response. This response is a full-body contraction dubbed a “sneeze”, a process that takes about 30 minutes and is used by the sponge to acquire oxygen, food and to excrete waste.

Ludeman et al. deactivated the non-motile osculum cilia by blocking cationic channels (shown to be crucial for primary cilia sensation in other metazoans) on these cilia. This channel-blocking lead to the reduction and elimination of the “sneeze”-response elicited by water flow. In separate trials, the researchers found that if the cilia were removed using chloral hydrate, or if the entire osculum itself was physically removed, then sponges stopped “sneezing”. By removing or deactivating the hypothesized sensory structures, the authors showed that sponges could no longer execute their normal flow-response behavior, the sneeze.

They found a new organ, so what?

Figure 1. Simple diagram of a demosponge body plan.

Figure 1. Simple diagram of a demosponge body plan.

Ludeman et al. claim to have identified a novel sensory organ in the freshwater sponge Ephydatia muelleri which is responsible for the transduction of sensory information from the flow of water in their environment, and aids in the coordination of full-body animal responses. Specifically, this species of freshwater sponge and other demosponges investigated, presented with ciliated cells lining the oscula, a feature not normally found in adult sponges (Fig. 1). Typically, ciliated cells are only found on larvae and thus the identification of an osculum entirely covered by ciliated epithelial cells is novel and evolutionarily distinct. While most sponges do not have the ability to trigger a sneeze in response to water flow, it appears that using their non-motile cilia, some demosponges can. This may help the organism clear sediment out of their osculum to prevent blockages in pores which may compromise nutrient acquisition.

In addition to identifying ciliated cells in a physical location not previously known, the orientation (perpendicular to water flow) of these cilia within the osculum indicates a potential mechanism for the detection of water flow.

The authors assume that the cilia present in the osculum are involved in sensation. The way in which the authors arrive at this conclusion requires some further reflection. Essentially, chemicals that have been shown to inhibit sensory ability of primary cilia in other organisms were used on the sponges, in an effort to elicit a behavioral change. Since the behavior of inflation and contraction was reduced by the application of two chemicals, and “sneezing” was completely suppressed when another chemical was applied, the researchers conclude that the structures have sensory function. There is some room for debate here as the most conservative conclusion would be that the inflation and contraction behavior simply requires the presence of a TRP channel. However, viven the ubiquity of TRP channels functioning in a sensory system it seems highly unlikely that these TRP channels are the only ones that do not have this function. Thus, it is assumed (with relatively high confidence) that these TRP channels serve a similar function to the other well-described TRP channels—a function in a sensory system.

What does this new sensory organ mean for our understanding of sensory evolution?

The non-motile cilia of the sponge osculum have a high surface-area to volume ratio and are similar to the primary cilia structures present in the more derived sensory systems of other metazoans. Primary cilia are optimized for sensing and transducing signals because of their high surface-area relative to volume. The ancient evolutionary history of poriferans makes an understanding of the structure, function, and evolution of their sensory structures a valuable insight into the evolution of later metazoan sensory systems. The TRP channels found on non-motile cilia of these demosponges are employed by a plethora of metazoan sensory systems including gustation, olfaction, temperature, vision and osmolarity. The cilia of sponges may be a basal form of the primary cilia present in other vertebrates, suggesting that early cilia functioned as flow detectors before being incorporated into other sensory structures in more derived metazoans. Alternatively, and by parsimony also plausible, non-motile cilia may have evolved convergently with the motile primary cilia of other non-poriferan metazoans. The location of demosponges indicates that if other poriferans possessed non-motile cilia, they have since lost them (Fig. 2). It is perhaps most likely that the freshwater group of Demospongia discussed in this study evolved the sensory cilia independently. As most sponges are marine organisms, the sensory cilia may not be beneficial to the majority in marine environments while it confers some evolutionary benefits to small groups in freshwater.

Figure 2. A basic cladogram of Porifera showing the presence of non-motive cilia in Demospongia.

Figure 2. A basic cladogram of Porifera showing the presence of non-motive cilia in Demospongia.

Questions we have for the authors, and scientific community:

With the new knowledge of ciliated epithelia of adult sponge osculum, many questions about the evolution of such features arise.

(1)  As sponge larvae have ciliated bodies to help them with mobility and it is known that adult sponges are sessile, it is likely that the loss of ciliated bodies during the transition to adulthood may be related to lack of function. It could be argued that as the presence of cilia on the endothelium is, as far as we know, restricted to freshwater sponges. If only freshwater sponges do indeed have these cilia, then specific aspects of the freshwater environment may be the reason the cilia are selected for and maintained in these demosponges.

(2)    Ludeman et al. demonstrated that the contraction response can be deactivated, but can it be triggered? Perhaps running behavioral tests where the “sneeze” is measured as variables such as water temperature, salinity, velocity, pressure, and sediment load are altered. This would develop our understanding of “why” freshwater sponges have non-motile cilia.

References

Ludeman DA, Farrar N, Riesgo A, Paps J, Leys SP 2014 Evolutionary origins of sensation in metazoans: Functional evidence for a new sensory organ in sponges. BMC Evol Biol 14(1):3. (DOI:10.1186/1471-2148-14-3)

 

 

 

 

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