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The Science of the Total Environment, 75 (1988) 271-283 271

Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

A C H E M O T A X O N O M I C S T U D Y OF D I T E R P E N E S F R O M M A R I N E
B R O W N A L G A E OF THE G E N U S D I C T Y O T A

VALERIA L. TEIXEIRA
Laboratorio de Botanica Marinha, Faculdade de Biologia e Psicologia maria Thereza, Rua
Viscone do Rio Branco 869, 24, 020 Niteroi, RJ (Brazil)

ALPHONSE KELECOM
Laboratory of Marine Natural Products, Departamento de Biologia Geral, Universidade Federal
Fluminense (UFF), C.P. 100.183, 24.000 Niteroi, RJ (Brazil)

ABSTRACT

Diterpenes from Dictyota species appear to be valuable taxonomic markers and showed, for
various species, strong correlation with botanic data. Our results corroborate the Theory of
Micromolecular Evolution that states that higher oxidation levels, in a given taxon, are charac-
teristic of evolutionarily more advanced components.

INTRODUCTION

P h a e o p h y t a are b r o w n algae, a l m o s t exclusively marine, litophylic, occa-


sionally epiphytic, and found p r i n c i p a l l y in cold and t e m p e r a t e w a t e r s [1]. The
division P h a e o p h y t a possesses one single class, P h a e o p h y c e a e , composed of
a b o u t 250 g e n e r a and m o r e t h a n 1500 species [2]. A c c o r d i n g to W y n n e and
L o i s e a u x [3], P h a e o p h y c e a e are d i s t r i b u t e d in 13 orders, two of which, F u c a l e s
and Dictyotales, are p r e d o m i n a n t in t r o p i c a l and sub-tropical seas [2].
The o r d e r D i c t y o t a l e s includes 16 fully defined g e n e r a [4]. A m o n g these, the
g e n e r a Dictyota L a m o u r o u x , D i l o p h u s J. Agardh, Glassophora J. Agardh,
P a c h y d i c t y o n J. Agardh, S p a t o g l o s s u m K u t z i n g and S t o e c h o s p e r m u m K u t z i n g
p r o d u c e a series of d i t e r p e n e s t h a t are p r o b a b l y involved in h e r b i v o r y c o n t r o l
[5, 6].
T h e genus Dictyota, with some 30 species, has been c h e m i c a l l y the most
e x t e n s i v e l y investigated: m o r e t h a n 90 d i t e r p e n e s of 17 skeletal classes h a v e
been isolated from 18 species d i s t r i b u t e d in all the o c e a n s [7]. Since problems
still exist in establishing the s e p a r a t i o n limits b e t w e e n species and v a r i e t i e s of
v a r i o u s Dictyota r e p r e s e n t a t i v e s [8, 9], it has been suggested t h a t the algae
d i t e r p e n e s m i g h t be of c h e m o t a x o n o m i c i n t e r e s t [10-12]. H o w e v e r , t h e r e h a v e
been no t a x o n o m i c n o r p h y l o g e n e t i c i n f e r e n c e s from the c h e m i c a l d a t a
r e s u l t i n g from the i s o l a t i o n and identification of d i t e r p e n e s from Dictyota
species. It is the aim of this w o r k to i l l u s t r a t e the g r e a t p o t e n t i a l of Dictyota
d i t e r p e n e s as c h e m o t a x o n o m i c and p h y l o g e n e t i c markers.
272
METHODOLOGY

Usually, chemosystematic studies are based on a presence/absence record of


metabolites [13]. It cannot be over emphasized, however, that such a criterion
may not be considered as fully reliable for chemotaxonomic purposes for at
least two reasons. First, because the presence of metabolites in an organism
may have been overlooked, and second because the isolation of known
compounds, even from new sources, is generally not reported (and even not
accepted for publication) in the main journals. Consequently, compounds that
are in fact present will be considered absent, and this may obviously alter the
chemotaxonomic conclusions. Hence, a methodology t h a t is not based on a
presence/absence criterion is necessary for the use of natural products in
taxonomy. Such a tool has been devised by O.R. Gottlieb [14] and has been
extensively used for this study.
Accordingly, all diterpenes isolated from Dictyota species up to June 1986
have been characterized by two indexes. First, the skeleton specialization
index (SI), calculated from the theoretical number of steps, involving C-C bond
formation or cleavage, that are necessary to derive a particular skeleton from
the common geranyl-geraniol precursor (see Figs 1-3). Second, the oxidation
index (OI), which considers identical all compounds having the same molecular
formulae and functionality irrespective of the isomer. Each Dictyota species
was then characterized by the skeletal evolutionary advancement index (EAs)
and by the mean oxidation index (OI), both obtained as the arithmetic mean
respectively of the SI and OI values of each diterpene isolated from considered
species. For a detailed description of the methodology, see Gottlieb [14].

RESULTS

The 17 diterpene skeletons obtained from Dictyota species are shown in Figs
1-3, and the number of diterpenes of each skeletal class is reported in Table 1.
The unidentified species for which chemical data are available were arbitrarily
numbered, in order to allow further discussion.
Based on a revised biogenetic scheme proposed by the present authors in an
earlier study [7], the diterpenes have been distributed into three groups (I-III),
depending on the first formal cyclization of the geranyl-geraniol precursor.
Diterpenes of Group I are mainly prenylated derivatives of known sesquiter-
pene skeletons t h a t result from a first cyclization of geranyl-geraniol between
positions 1 and 10 (Fig. 1). Group II contains diterpenes derived by a cyclization
of the precursor between positions 1 and 11 (Fig. 2). With the exception of the
dolabellane skeleton, the diterpene skeletons of this group are restricted,
among Dictyotales, to Groups I and III. Whether or not D. spinulosa, for which
only one xeniane-related diterpene had been reported [12], belongs to the latter
group will be discussed later. Finally, the cosmopolite D. dichotoma [2], which
is considered to be the type species of the genus [4], is the only species that
produced diterpenes from all three groups [13-55].
Our results, obtained by numerical treatment using the mean oxidation (OI)
273

I m ~ !
"7
=

;" e
q

%1
c-a

o.~ o ~g ~

v- 0 c~

~b
et
274

~
all-trans-
geranyl-geraniol
I,ii

?2,7
pyrophosphate

i0

I dictymane secodolastane 4

\
seco 10,14

/ dolabellane
08} 8 ~,7
I
H

dolastane 17
dictyoxetane I

Fig. 2. Hypothetical biosynthetic pathway for Dictyota diterpenes of Group II.

and the mean skeletal evolutive advancement (EAs) indexes for all the Dictyota
species considered in this work, are reported in Fig. 4.
The A area includes species that yield exclusively diterpenes from Group I.
These are characterized by low OI (~ - 1.43) and EAs (~ 0.10) values. Dictyota
masonii was tentatively included (dotted line) in sub-group A for having only
one diterpene reported [19] whose OI and EAs indexes (OI = - 1 . 5 0 ;
EAs = 0.05) were found to be in discrepancy with the values observed for the
other species of sub-group A.
Sub-group B corresponds to species that produce diterpenes belonging ex-
clusively to Group II. Their main characteristics are high OI (~ 1.26) and
EAs (~ 0.15) values. Among these species, Dictyota sp 1 is peculiar in being the
275

al i- trans-geranyl-geraniol
pyrophosphate

2 1

crenulidane ]

i
i

tricyc lodictyotane 3 dichotomane 2

Fig. 3. Hypothetical biosynthetic pathway for Dictyota diterpenes of Group III.


only one that afforded dolabellanes, when all the other species yielded
dolastanes.
Sub-group C includes the algae that furnish diterpenes from Groups I and III.
T h i s s u b - g r o u p is c h a r a c t e r i z e d by t h e l o w e s t E A s v a l u e ( ~ 0.09) a n d by a n OI
v a l u e of - 1.32. In t h i s s u b - g r o u p , Dictyota prolificans is d i s c r e p a n t for h a v i n g
276

oumoXaa~poIaXaTaJ,

aumuoaoqa!G

au~p!Inuaa~3

auNnuaa~)

au~.tuoxoIa£ D

oue!ua X

oum, oxoXaa!(l

ou'~m£~,a!G

au~:ls~IoG-oaos
ou-elSe,lO(l

ou~Iioqe.lO(l

OU~lmaKI

pol~I£uoad
au~aamuaa~olaXa!EI
au~1o£aa!(I
paa~l£uaad
~a ou~!en D

..= poa~IuXoad
aumuoIo-p!dkl
po1~I£uaad
ou~Imuap!aa O
pa:~uI£uaad
OulgaDl~U.laO D

"B

gn
< i X
O3
277

a high OI value ( - 1.07), very different from the mean value of its sub-group.
Two species, D. spinulosa and D. dichotoma, could not be included in any of
these sub-groups. The former due to poor phytochemical information available
when we started this study (but see Discussion); the latter since it yielded
diterpenes of all three Groups I-III. This may be related to the fact t hat the
plant material used for this chemical investigation had been collected from
several regions of the world, or more probably because this alga, due to its
great morphological variability and to badly defined limits, may in fact include
a complex of species [9].
It should be noted t hat the species with the highest EAs values, produced,
in general, the most functionalized diterpenes, i.e. had high OI values (species
from sub-group B). Among these species, Dictyota cervicornis, from Brazil,
showed the highest OI as well as EAs indexes.

DISCUSSION AND CONCLUSIONS

According to botanists, Dictyota acutiloba is a fully characterized species


with well-defined limits [56]. The geographic distribution of this species is
restricted to the Pacific tropical waters [56]. As mentioned above, D. acutiloba
furnished diterpenes whose skeletons have not been found in any other species
of the genus. All this may indicate an early independent evolutionary process.
The four unidentified Dictyota species (numbered from 2 to 5) cannot be
correlated with botanical data. However, they all seem to belong to this genus
as far as the OI and EAs indexes are concerned (Fig. 4). Dictyota sp 1 is
characterized by the presence of dolabellanes and not dolastanes as observed
for all the other species in sub-group B. This fact led us to suspect t hat the
taxonomical classification of this alga was wrong. Indeed, when this work was
underway, the alga "Dictyota sp 1" was submitted to a novel biological classi-
fication and turned out to be actually a species of the genus Dilophus [33].
The poor phytochemical informatioin available for Dictyota dentata, D.
indica and D. flabellata do not allow any correlation with botanical data;
several of these species present taxonomic problems [8].
The OI and EAs indexes calculated for Dictyota prolificans were found to be
very different from the mean values observed for sub-group C. This observation
strongly suggested t ha t D. prolificans should not be included among the rep-
resentatives of the genus Dictyota. Our assumption was in agreement with a
recent botanical revision [56]. Indeed, Allender and Kraft, investigating the
Australian Dictyotaceae, observed t ha t Dilophus prolificans (the alga from
which prenylated bicyclogermacranes were isolated [41]) corresponded to the
same plant as Dictyota prolificans. From morphological and reproductive
studies, the authors adduced the synonymy, and included these specimens in a
new combination, Dilophus intermedius (Zanardini) Allender and Kraft [56].
This is a typical example of a problem t hat would have been overlooked by a
conventional study based on the presence or absence of metabolites, since the
target compounds were in fact present, but their mean oxidation index was too
small.
278

OI

-1.O

12
I%

I %%
l %
I
I %%
I
0 ;| ~%
13 ' '% 7 . ~ e3
4'o , ;0,../
8 • ~ e 6
2 o5
.A
-1.4
. -" =, A17
.-'"'" _ . . . . --'~---'~i
&...'_ . . . . . . .
11

-i.£

0.05 0.10 0.15 E~


s

Fig. 4. M e a n oxidation indexes (O]) versus evolutive advancement skeleton indexes (~B) for
Dictyota species. (1) Dictyota acutiloba ( 1.45, 0.13), (2) Dictyota binghamiae (-1.32, 0.09), (3)
Dictyota cervicornis ( - 1.21, 0.17), (4) Dictyota crenulata ( 1.26, 0.08), (5) Dictyota dentata ( - 1.39,
0.10), (6) Dictyota dichotoma (-1.38, 0.10), (7) Dictyota divaricata (-1.24, 0.15), (8) Dictyota
flabellata ( - 1.35, 0.08), (9) Dictyota indica ( - 1.40, 0.10), (10) Dictyota acutiloba ( - 1.45, 0.13), (11)
Dictyota masonii ( - 1.50, 0.05), (12) Dictyota prolificans ( - 1.07, 0.07), (13) Dictyota spinulosa ( - 1.20,
0.05), (14) Dictyota sp 1 ( - 1.34, 0.10), (15) Dictyota sp 2 ( 1.33,0.09), (16) Dictyota sp 3 ( - 1.27, 0.15),
(17) Dictyota sp 4 ( - 1.43, 0.13), (18) Dictyota sp 5 ( - 1.43, 0.11).
D a w s o n [8] c o n s i d e r s D i c t y o t a b i n g h a m i a e to be s y n o n y m o u s w i t h Pachydic-
tyon coriaceum. T h e f o r m e r a l g a p r o d u c e s d i t e r p e n e s of the x e n i a n e a n d of the
p r e n y l a t e d g u a i a n e s k e l e t o n s , w h e r e a s P. coriaceum yields, in addition,
d i t e r p e n e s of G r o u p II [7]. T h i s o b s e r v a t i o n c o n t r a d i c t s D a w s o n ' s proposal.
D i c t y o t a cervicornis, D. d i v a r i c a t a a n d D. linearis, c h a r a c t e r i z e d c h e m i c a l l y
by the p r e s e n c e of d o l a s t a n e s , are c o n s i d e r e d by b o t a n i s t s to be m o r p h o l o g i -
cally v e r y s i m i l a r [57]. O u r d a t a a g r e e w i t h this a s s u m p t i o n . D i c t y o t a sp 3 (from
the C a n a r y Islands) m a y be one of t h e s e t h r e e species, w h i c h a r e w i d e s p r e a d in
this a r e a [58].
N i z a m m u d d i n a n d Gerloff [59] c o n s i d e r Dictyota crenulata, f r o m the r e g i o n
w h e r e this a l g a h a d b e e n collected for c h e m i c a l i n v e s t i g a t i o n , to be D i l o p h u s
c r e n u l a t u s (J. Agardh). O u r d a t a r e v e a l t h a t the e x c l u s i o n of this species from
t h e g e n u s D i c t y o t a a n d its i n c l u s i o n in t h e g e n u s D i l o p h u s should be pre-
279

cipitated, since the diterpene skeletons from Dictyota crenulata (crenulane and
crenulidane) have been observed not only in Dilophus okamurai [60], but also
in Pachydictyon coriaceum [61].
It is interesting to note that, with the exception of Dictyota spinulosa, for
which limited phytochemical data was available when we started this study, all
the species that produce diterpenes from Group III also produce diterpenes
from Group I (i.e. sub-group C). this may indicate that the early biosynthetic
steps leading to these two classes of diterpenes are common, and hence that the
xeniane skeleton does not derive from a first anti-Markovnikov cyclization of
geranyl-geraniol between C-2 and C-10 as is generally accepted [62] and as we
depict in Fig. 1. Recently, Kakisawa et al. [63] proposed that xenianes are
derived by ring contraction of a prenylated germacrane precursor. This
proposal is in agreement with, and is corroborated by, our observations. From
all this, it was tempting to speculate on the presence, in D. spinulosa, of
diterpenes of Group I in addition to the already reported xeniane-type
compound. A recent report [64] has confirmed this hypothesis and indicated
that D. spinulosa belongs indeed to sub-group C.
Finally, from the co-occurrence of dolabellane, dolastane and dictalane in
an unidentified species of Dictyota from the Canary Islands, it has been
proposed, in a preliminary communication [65], that the dictalane skeleton
may derive from cyclization and rearrangement of a dolabellane precursor. If
this is true, the dictalane skeleton should belong to Group II and not to Group
I. Although coherent, a full paper has not yet appeared on this biosynthetic
proposal. However, since there are no other records of the co-occurrence of
dolabellanes and dolastanes, it is not impossible t h a t these results can be
explained by a possible heterogeneity of the studied Dictyota sample. In this
respect, one should note t h a t Dictyota dichotoma is the only species identified
that yielded dolabellanes together with diterpenes of 10 other skeletons. But,
even in this particulalry rich species, dolastanes do not co-occur with dola-
bellanes.
All this indicates that diterpenes appear to be good taxonomic markers for
the genus Dictyota, showing for various species strong correlations with
botanic data. In addition, the lack of experimental biosynthetic work is also
evident.
Moreover, our results corroborate Gottlieb's Theory of Micromolecular
Evolution [14], which states that higher oxidation levels are characteristic of
evolutionarily more advanced components of a given taxon (first part of the
Second Principle of Micromolecular Evolution). Hence, among the species that
were studied chemically, the representatives of sub-group B (Fig. 4) appear to
be the most evolved of the genus.

EXPERIMENTAL

OI and EAs indexes were calculated following Gottlieb [14]. Dictyota


acutiloba (IO = - 1.45; EAs = 0.13), D. binghamiae ( - 1.35; 0.09), D. cervicor-
280

nis (-1.22; 0.16), D. crenulata (-1.26; 0.08), D. dentata (-1.39; 0.10), D.


dichotoma ( - 1.38; 0.10), D. divaricata ( 1.23; 0.15), D. flabellata ( - 1.35; 0.08),
D. indica (-1.40; 0.10), D. linearis ( 1.30; 0.15), D. masonii (-1.50; 0.05), D .
prolificans (-1.07; 0.07), D. divaricata (-1.20; 0.05 corrected including
d i t e r p e n e s r e p o r t e d i n r e f . 64: - 1.34; 0.06), Dictyota sp 1 ( - 1.34; 0.10), Dictyota
sp 2 ( - 1.33; 0.09), Dictyota sp 3 ( - 1.27; 0.15), Dictyota sp 4 ( - 1.43; 0.13) a n d
Dictyota sp 5 ( - 1.42; 0.11).

ACKNOWLEDGEMENTS

This work was financially supported by CAPES, FINEP and CNPq grants.
V.L.T. thanks the Conselho Nacional de Desenvolvimento Cientifico e Tec-
nologico (CNPq) for a fellowship.

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