Algal photosensory apparatus probably represent multiple parallel evolutions

BioSystems, 16 (1983) 31--38 Elsevier Scientific Fublishers Ireland Ltd.

31

A L G A L P H O T O S E N S O R Y APPARATUS PRO BA BL Y R E P R E S E N T M U L T I P L E P A R A L L E L EVOLUTIONS

PETER A. KIVIC and PATRICIA L. WALNE Department of Botany, University of Tennessee, Knoxville, TN 37996-1100, U.S.A. (Received July 8th, 1982) (Revision received September 24th, 1982) We postulate that algal photoresponse mechanisms are of relatively recent origin and represent numerous parallel evolutions. Functional differences among them are evident, and it is unlikely that any one can be taken as a "model system" representing all. It is probable that the light antenna is the only truly novel part of the apparatus in most cases, with the signal-processing and motile elements being borrowed from some other, more ancient, sensory system. It is thus anticipated that the light-antennae will show the greatest phylogenetic variation, whereas the :dgnal-processors and motile elements will resemble those of other sensory systems in the same groups of organisms. Light-seeking behavior is virtually universal among motile algae. As an adaptive activity, it allows organisms to relocate wherever the light intensity best meets their p h o t o s y n t h e t i c requirements. P h oto tactic machinery necessarily consists o f three basic c o m p o n e n t s : (a) a photor e c e p t o r and associated light-modifying accessories; (b) an effector, which causes the cell to move toward or away f r om the light; and (c) a signal--processing and transmitting system, which translates and transmits the p h o t o r e c e p t o r o u t p u t t o the effector. In phytoflagellates, where m os t of the photoresponse studie.~ have been carrried o u t thus far, the m o s t p r o m i n e n t part of the entire apparatus is generally the stigma, presumed to be one of the accessory structures (Foster and Smyth, 1980). The photor e c e p to r itself is m uc h less conspicuous; it has been tenl~atively identified in a few organisms with one or a not he r smaller structures near the stigma. The effector, at least in phytoflagellates, m ay be e xpe c t e d to be one o f the contractile elements associated with the flagellum, e.g. the a x o n e m e or a flagellar root, since steering is invariably

via alterations of flageUar orientation and/ or activity. Even less is presently known about the signal-processor; at this stage it is chiefly a h y p o t h e t i c a l c o n c e p t (see e.g., Diehn, 1973; O m odeo, 1980). Some authors express the aim of finding a c o m m o n mechanism for p h o t o r e c e p t i o n (e.g., Colombetti and Lenci, 1980; Omodeo, 1980; Tollin, 1969), or the h o p e of establishing some particular organism as a " m o d e l s y s t e m " of neurosensory behavior (e.g., Diehn, 1973; Wolken, 1967, 1977). We suggest here, however, t h a t there is no universal " m o d e l system". It is anticipated, rather, t hat these algal p h o t o t a c t i c mechanisms will prove to be a collection o f several parallel evolutions, t hat t h e y will be f o u n d to operate on som ew hat different principles, and t hat whatever t h e y do have in c o m m o n is dictated by c o m m o n evolutionary pressures operating on somewhat similar organisms.

SET implications concerning evolution of the photosensory apparatus T he

0303-2647/83/$03.00 © Elsevier Scientific Publishers Ireland Ltd. Printed and Published in Ireland

basis

for these conclusions is the

32 Serial Endosymbiosis Theory (Goks~byr, 1967; Margulis, 1968, 1970) which postulates, among other things, that the chloroplast originated from a photosynthetic prokaryotic endosymbiont residing within an otherwise animal-like eukaryotic protist. Previous discussions of the SET have been devoted largely to arguments concerning its validity (see, e.g., Allsop, 1969; Gray and Doolittle, 1982; Klein and Cronquist, 1967; Lee, 1972; Raven, 1970; Schnepf and Brown, 1971); by now, however, it appears to be generally accepted. We therefore begin here with the SET as our initial hypothesis, and examine some rather interesting implications it has regarding phototactic mechansims. First, the light, seeking algal photoreceptor may be considered a relatively recent structural innovation, at least compared to the rest of the cell. As a functional adjunct of the chloroplast, its origin would have necessarily followed chloroplast acquisition (but, see the discussions below of Stentor, and of the dinoflagellate ocellus), which is itself hypothesized to be a relatively late event in eukaryote origination (e.g., Margulis, 1968, 1970; Taylor, 1974). Second, the phototactic mechanism may have evolved fairly quickly. The newly photosynthetic eukaryote would have been subjected to a selective pressure either to optimize the usefulness of its new chloroplast, or to lose it. Possibly the most expedient way to achieve optimal photosynthetic capability in a motile uniceU would be to develop a light, seeking capacity. Third, the evolution of light-seeking behavior probably happened many times over. It has been argued that plastids were "re-invented" at least three times, to form the groups of green, red, and yellow-brown algae, respectively (Raven 1970; Margulis, 1970). To this list one should probably add the blue-green cyanelles (Taylor, 1974), which alone very likely represent a halfdozen or so separate symbioses (Fogg et al., 1973). Finally, some types of algae apparent-

ly originated by a somewhat different process: a protist endosymbiotically incorporating another protist that already possessed a plastid (see Tomas and Cox, 1973; Gillott and Gibbs, 1980; Bujak and Williams, 1981). Each of these newly photosynthetic organisms would have been subjected to the same evolutionary pressure to form its own separate phototactic device.

Algal photoreceptors represent many different mechanisms It is unlikely that all of these photoresponsive apparatus would have arisen in precisely the same way, or would have used exactly the same mode of operation. It could be hypothesized that the physiological and structural similarities among them would be no greater than that imposed by the common functional requirements and the limited differences in the "starting materials". Studies carried out on the ultrastructure and physiology of algal photosensory mechanisms seem to bear this out. In their detailed review, Foster and Smyth (1980) demonstrated that phytoflagellate light receptors are broadly alike in that they are all rotating light, antennae, but that their light-processing strategies and attendant fine structural modifications show a wide range of variation. Similarly, in Euglena and Chlamydomonas, the two algae in which phototactic responses have been most extensively studied, the signal transduction mechanisms are roughly similar in that both are mediated by a transient trans-membrane Ca2*-ion influx, but the details of the processes appear to differ greatly (see Table 1; also Colombetti and Lenci, 1980; Haupt, 1980). The nature of the phototactic response varies as well. Chlamydomonas, Volvox (Feinleib, 1980), and Gyrodinium (Hand and Schmidt, 1975) exhibit a "stop" reaction in response to an increase in light intensity; Euglena shows a "shock" reaction (spinning in situ) in response to a decrease in light

33 TABLE 1 C o m p a r i s o n o f t h e Ca~+-mediated p h o t o t a c t i c r e s p o n s e s o f

M i n i m u m Ca ~÷ i n f l u x r e q u i r e d to trigger a r e s p o n s e T y p e o f r e s p o n s e triLggered Light stimulus reqmred E f f e c t o f La 2÷ E f f e c t o f Mg 2÷ E f f e c t o f Co 2. E f f e c t o f Ba 2÷ Effect of procaine References

Euglena a n d Chlamydornonas

Euglena

Chlamydomonas

> 10 -a M

> 10 -~ M

Flagellar position altered Decrease in intensity Blocks response Nil Increased klinokinesis Partially substitutes for Ca 2÷ Nil Doughty and Diehn, 1979 Doughty et al., 1980

Flagellar b e a t reversed Increase in i n t e n s i t y Nil Blocks r e s p o n s e Nil Blocks r e s p o n s e Blocks r e s p o n s e S c h m i d t a n d Eckert, 1 9 7 6

intensity (Diehn, 1973); Cryptomonas (Watanabe and Furuya, 1982) and the non-flagellate Porphyridi~m (Schuchart, 1980) have no such dramatic responses at all to changes in illumination; they just orient slowly and continuously toward the light.

How m a n y times did algal photoreception evolve? Based upon their structural diversity, it should be possible to estimate at least a minimum number of times that algal phototactic mechanisms came about. For this purpose the following assumptions are made: (a) each initial plastid acquisition, perhaps represented at present by the green, red, and yellow-brown plastids and the blue-green cyanelles, as well as each secondary plastid acquisition via endosymbiosis of a plastid-containing eukaryote, would probably be followed by the subsequent evolution of one or more photosensory mechanisms; (b) within each of these groups, the presence of different Foster-Smyth lightantenna types would indicate separate evolutions of phototactic apparatus (this is a[so the conclusion reached

by Foster and Smyth (1980) and was suggested as well by Halldal (1958)); and,

(c) even within

a single light.antenna type there may be two or more distinct stigmatal morphologies (sensu Dodge, 1973), and each of these probably represents an independent photoreceptor origin; thus the minimum number of parallel evolutions to be accounted for becomes multiplied still further.

Counting each stigma type of each light" antenna type of each plastid type (and more parameters could probably be added if one wished to carry the argument even further), it can be seen, as shown in Table 2, that algal photoreceptors must have arisen independently ten or more times. This would provide at least a partial answer to the question raised by Colombetti and Lenci (1980) as to why there are six or more different types of photoreceptor pigments in photomotile microorganisms. It may be noted that two of the lightseeking algae listed in Table 2, the rhodophycean Porphyridium and the cyanellecontaining Paulinella, are ameboid forms, thus showing that the evolution of phototactic devices is not limited to phytoflagellates.

34 TABLE 2 Examples o f morphologically distinct algal photoreceptor types representing probable independent evolutions Phylum

Organism

Plastid color

Eyespot type (after Dodge, 1973)

Light-antenna type (after Foster and Smyth, 1980)

Chlorophyta

Chlamydomonas

Green

A

Multilayer quarter-wave stack

Probable independent photoreceptor evolutions 1

Prasinophyta

Platymonas

Green

A

Multilayer quarter-wave stack

Cryptophyta

Chroomonas

Yellow-Brown

A

Dielectric slab wave guide

2 3

Dinophyta

Peridinium westii

Yellow-Brown

A

Quarter-wave stack

Chrysophyta

Ochromonas

Yellow-Brown

B

Absorbing screen and paraflagellar b u t t o n (type I)

Phaeophyta

Fucus (gamete)

Yellow-Brown

B

Absorbing screen and paraflagellar button (type I)

4

Xanthophyta

Heterococcus

Yellow-Brown

B

Absorbing screen and paraflagellar button (type I)

Haptophyta

Pavlova

Yellow-Brown

B

Absorbing screen and paraflagellar button (type II)

5

Absorbing screen and dichroic crystal detector

6

Absorbing screen and paraflagellar button

7

Euglenophyta

Eustigmatophyta

Euglena

Polydriella

Green

Yellow-Brown

C

C

Dinophyta

Wolozynskia coronata Yellow-Brown

C

Single-layer quarter-wave stack 8

Dinophyta

Glenodinium

D

(Multilayer quarter-wave stack? )

Yellow-Brown

Rhodophyta

Porphyridium

Red

Dinophyta

Ceratium

Yellow-Brown

Dinophyta

Erethropsis

None

(Cyanelle-bearing Paulinella rhizopod)

Blue-Green

--

E -

9

Unknown

10

Unknown

?

Lens, retina, and quarter-wave stack

--

Unknown

11?

35 Photosensory apparatus may have evolved from pre-existing: mechanisms A point worth further consideration is the nature of the "starting materials" available for the evolution of a light-seeking mechanism. These would consist of: (a) the new plastid, with its lamellar substructure and carotenoid-synthesizing capabilities, among other characteristics; and (b) the animal-like protist host cell, with its builtAn motile machinery, and most importantly, an already-established repetoire of kinetic and tactic responses to a number of environmental variables, (e.g., touch, gravity, food, toxins). This means that it was unnecessary for the newly photosynthetic cell to develop its light-seeking apparatus completely de novo. A far simpler alternative would have been to exploil~ one of these pre-existing response mechanisms, adding on to it a directional ante~ana to acquire the required light-sensing capability. There is, in fact, precedent for this suggestion. Precisely the same phenomenon, the usurpation of another sensory system for light-seeking purposes following the introduction o:[ photosynthetic capacity, has already been postulated for the green paramecium, P. bursaria, which carries endosymbiotic Chlo~ella cells (Cronkite and Van den Brink, 19131). Further afield, similar evolutionary modifications of chemosensory systems to make directional photoreceptors, (in these cases, light-avoiding photosensory mechanisms not, related to photosynthesis) have been reported in a nematode (Burr, 1979}, and a n~n-photosynthetic bacterium (Taylor, 1979). It is even pos.,~ible (albeit unlikely) that the light antenna as well evolved prior to chloroplast acquisition, in some instances. Two presently hypothetical situations can be noted in which the light antenna might not have originated strictly de novo, but was included, in whole or in part, among the algal cell's "starting materials". (a) It might have pre-existed as part of

the animal-like precursor protist. It is possible that an algal photoresponse apparatus will be found which predates the plastid itself. Some animallike protists (e.g., the ciliate Stentor, Song, 1981; Song et al., 1980), have well-developed light-orienting mechanisms of their own; such a cell could have served, conceivably, as the host for a plastid acquisition. A similar example is the group of ocellus-containing dinoflagellates represented in Table 2 by Erethropsis. Both Dodge (1969) and Foster and Smyth (1980) treat this lens-containing organelle as an algal photoreceptor; however, these organisms are not chloroplast-containing autotrophs but predators, and it is probable that the ocellus is not a light-seeking device, but a shadowtriggered prey sensor (Omodeo, 1980). It would be interesting to know what phylogenetic relationships, if any, this device has to the light-seeking mechanisms of Erethropsis' photosynthetic relatives. (b) The photoreceptor could have entered the cell as a part of the original photosynthetic endosymbiont in those algal groups, such as cryptophytes (Gillott and Gibbs, 1980) and certain dinoflagellates (see Bujak and Williams, 1981), in which the chloroplast represents the endosymbiosis, not of a prokaryote, but of another plastidcontaining algal cell. In at least three dinoflagellates (Dodge, 1971; Jeffrey and Vesk, 1976; Tomas and Cox, 1973) and one cryptophyte (Lucas, 1982) it appears that at least part of the phototactic apparatus is derived from the pre-existing phototactic apparatus of the algal endosymbiont. It is anticipated, then, that in any given algal group or sub-group, the photoreceptor system will be found to resemble some other response mechanism in this same organism (and indeed, in some non-photo-

36 synthetic relatives) more than it will the photoreceptor system of another group of algae. To this point it can be noted that the euglenoid flagellum has both a thigmotactic response (cf. Lowndes, 1944; Chen, 1950; Mikolajczyk and Diehn, 1976) and a chemosensory response (Colombetti and Diehn, 1978) resembling its phototactic response. The various elements of the photosensory mechanism would have had different origins A further implication is that the different parts of the phototactic apparatus would have had different evolutionary histories. In most instances the " y o u n g e s t " part of the system would be the light-antenna (i.e., the photoreceptor and its attendant lightprocessing accessories such as the stigma); these were presumably the only pieces that were not already in place before photosensory behavior arose. In the chlorophytes, prasinophytes, chrysophytes, xanthophytes and phaeophytes, there is no doubt that the stigma arose only subsequent to plastid acquisition; in each case, it is part of the plastid (Dodge, 1973). The light-antenna/ photoreceptor/accessories would therefore be expected to show greater variation than other elements of the photoresponse machinery. Conversely, the motile elements (e.g., the axoneme and flagellar roots, in the case of most phytoflagellates) would probably be the "oldest" part of the system, possibly pre-dating any control mechanism, and would thus be evolutionarily very conservative. The intervening control mechanism, which processes the light signal and modifies the pattern of motility, is the least-known part of the system; as stated above, we anticipate that in most cases it will be found to resemble the control mechanism for some other sensory response in the same organism. It will probably be less variable from group to group than are the light-antennae. Some of these control mechanisms may even

reflect a c o m m o n ancestry extending back to a period far pre~lating the origins of plastids and algal photoreceptors. They probably will not be as conservative as the motile elements, however. An alternative, less probable, scenario which must still be considered as a possibility is that the entire photosensory apparatus was already in place (in, e.g., an Erethropsis-like host cell) prior to chloroplast acquisition. No examples of this are readily available, however. Conclusions It is likely, then, that algal phototactic devices, with perhaps a few exceptions, are of relatively recent origin (in evolutionary terms), and represent m a n y parallel evolutions. As might be anticipated, they show numerous ultrastructural, and probably physiological, differences reflecting their basically different operational strategies. It is unlikely that any of these devices originated strictly de novo; more likely, each is a modification of some other pre-existing sensory system. The photoreceptors and the accessory structures modifying the light signal are, therefore, expected to show more phylogenetic variability than will the signal-transducing mechanisms, and the latter, it is anticipated, will also resemble other sensory signal-transduction mechanisms in the same organisms. It would appear unlikely, then, that any one organism could be taken as a universal " m o d e l system" representing the entire lot. At best, it might represent sensory behavior within its own phylum or class or order. A broad understanding of photosensory behavior in general will probably come only from a comparison of a number of these primitive photoresponsive organisms. Acknowledgement This work was supported by N.S.F. Grant No. DEB 7820210 to P.L.W.

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