Download An optional C-terminal domain is ancestral in α

Amylase 2017; 1: 26–34
Research Article
Open Access
Jean-Luc Da Lage*
An optional C-terminal domain is ancestral
in α-amylases of bilaterian animals
DOI 10.1515/amylase-2017-0003
Received February 17, 2017; accepted March 28, 2017
Abstract: The modular structure and organization of
most proteins is a fascinating aspect of their origin and
evolution. α-Amylases are known to be formed of at least
three domains. In a number of bacterial α-amylases,
one or several additional domains may exist, which are
carbohydrate binding modules, interacting with raw
substrates. In animal α-amylases, however, no additional
domain has been described. Here we report the presence
of a C-terminal domain, previously described only in the
bacterium Pseudoalteromonas haloplanktis. This domain
is widely distributed in invertebrate α-amylases and
must be ancestral, although it has been lost in important
phyla or groups, such as vertebrates and insects. Its
function is still unknown. In a single genome, enzymes
with and without the terminal domain may coexist. In a
few instances, this domain has been recruited by other
proteins in both bacteria and animals through domain
shuffling.
Keywords: domain shuffling; evolution; intron;
horizontal gene transfer; carbohydrate binding module
Abbreviations: AHA, Pseudoalteromonas haloplanktis
α-amylase; CBM, carbohydrate binding module; SBD,
starch binding domain.
1 Introduction
Protein evolution and innovation often goes about through
admixture of existing materials, such as pieces of existing
proteins, often fully functional domains. Countless
examples have been described, such as muscular proteins,
*Corresponding author: Jean-Luc Da Lage, Evolution, Génomes,
Comportement, Ecologie, CNRS, IRD, Univ Paris-Sud, Université
Paris-Saclay, F-91198 Gif-sur-Yvette, France;
E-mail: [email protected]
immunoglobulins and enzymes (for details, see, e.g. [1]).
The design and building of novel proteins often rely on
exon shuffling, in which introns serve as linking regions
between the pieces to be joined. This process, which had
been predicted by Walter Gilbert in his seminal article [2],
is quite common in Eukaryotes, especially in Vertebrates,
but has also been exemplified, for example, as a recent
event in Drosophila [3]. The domains, joined together,
may be tightly linked or attached to each other by a low
complexity protein region named a linker. However,
introns are not necessary, since domain shuffling may
also occur in Prokaryotes, which are devoid of introns (see
below).
α-Amylase plays a crucial role to achieve the
hydrolysis of starch and other polysaccharides from food
and nutrients into maltose and maltodextrines. Although
amino acid sequences are highly variable among
organisms, the general tertiary structure is well conserved.
It is made of a “(β/α)8 barrel” or “TIM barrel” (domain A),
a protruding few structured domain B involved in Ca2+ ion
binding and catalysis at the interface with domain A, and
an all-β domain C adopting a Greek key conformation.
In about 10% of bacterial and fungal α-amylases
and related enzymes, an additional terminal domain is
present, sometimes in N-terminal position, but most often
in C-terminal position, with a function of raw or granular
starch-binding, hence its name of starch binding domain
(SBD) [4-6]. SBDs belong mainly to the carbohydrate
binding module (CBM) families 20, 21, 25, 26, 34, 41, 45, 48,
53, 58, 68 and 69 ([7], http://www.cazy.org/). They consist
of all-β domains forming an open, distorted β-barrel, with
binding sites for polysaccharides, which use conserved
tryptophan residues.
A different, unrelated additional C-terminal domain
has been described from a bacterium, Pseudoalteromonas
haloplanktis,
which
is
an
antarctic,
marine
γ-proteobacterium (Alteromonadaceae). Its unique
α-amylase (AHA), which is adapted to cold temperature,
has been extensively studied (e.g. [8-11]). Its amino acid
sequence is strongly related to animal ones, and we have
suggested that AHA and animal (bilaterian) α-amylases
© 2017 Jean-Luc Da Lage, published by De Gruyter Open.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 License.
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could be related to each others through a lateral transfer,
whose direction is still not ascertained, but more likely
from bacteria to bilaterians [12,13]. AHA possesses an
original C-terminal domain, unrelated to SBDs, and not
yet ascribed to any family, which has been shown to act
possibly as a secretion helper, cleaved from the core enzyme
by a non-specific protease after exportation across the
outer cell wall [10]. Within the bacterial kingdom, we had
previously found this “propeptide” domain only in a few
species of the Pseudoalteromonas genus, and also in the
bacterium Saccharophagus degradans (Cellvibrionaceae,
formerly ascribed to Alteromonadaceae). In the latter
case, the C-terminal domain was attached to a plantlike α-amylase, but not to the orthologous animal-like
α-amylase, which also exists in this species, showing an
example of domain translocation and shuffling without
the need of an intron [12]. In animals, however, no
extra domain had been characterized until now. In fact,
sequence similarity between the AHA C-terminal domain
and an animal sequence had been only noticed [10] in
Caenorhabditis elegans.
In the present study, we show that this domain not only
exists in animals, but is widespread, and thus is probably
ancestral in bilaterians. The long-standing presence of this
domain in various non-vertebrate animals suggests that it
has a function. Although this hypothetic function cannot
be reached for now, we draw an evolutionary history of
this uncharacterized, yet quite common, protein domain.
2 Materials and methods
2.1 Experimental data
We checked the presence of a C-terminal domain
experimentally in several molluscan species. The
α-amylase genes were entirely sequenced in the bivalves
Corbicula fluminea and Mytilus edulis, and almost
entirely in the limpet Patella vulgata, using the Genome
walker Universal kit (Clontech). The C-terminal domains
were identified by BLAST search [14] in the GenBank
database. From the alignment of these domains with
those of P. haloplanktis, S. degradans and C. elegans, we
designed PCR primers in conserved parts of the domain
(Ctermdir:
CARGAYCTNTTYATHCGNGG;
Ctermrev:
TCNGCNCCRTACCARTC) and used various combinations
for amplification of fragments, if possible showing
attachment to the core α-amylase sequence, i.e. also
using primers designed within the core enzyme. The
species assayed by PCR were the chiton Acantochitona sp.
(Mollusca, Polyplacophora) and the oyster Crassostrea
C-terminal α-amylase domain in animals
27
gigas (Mollusca, Bivalvia). Sequence data were deposited
in GenBank (accession numbers are indicated in Table S1).
2.2 Searches in databases
Using the putative C-terminal domains of C. fluminea or
AHA as a query, we searched by BLASTP and TBLASTN [14]
in sequence databases for other occurrences of domains
similar to the AHA C-terminal domain. The GenBank nr,
GenBank EST and GenBank Bacterial genomes databases
(http://blast.ncbi.nlm.nih.gov/Blast.cgi) were searched.
We investigated traces archives at the NCBI for nonvertebrate metazoans. More specific genome servers were
also used: the EchinoBase server (http://www.echinobase.
org/) for echinoderms; server of the Joint Genome Institute
(http://genome.jgi.doe.gov/) for Daphnia pulex, Capitella
teleta, Lottia gigantea, Branchiostoma floridae, Helobdella
robusta and Ciona intestinalis; specific servers for the
Aplysia californica EST project (http://aplysia.cu-genome.
org/) and the nematode Pristionchus pacificus (http://
www.pristionchus.org/);
nematode-specific
servers
(http://www.nematode.net/); the “neglected genomes”
database
(http://www.nematodes.org/bioinformatics/
databases.shtml); also for marine organisms (http://www.
marinegenomics.org/); for the Urochordate Oikopleura
dioica (http://www.genoscope.cns.fr/); for the tick
Ixodes scapularis (http://www.vectorbase.org/); and
the InsectBase for various insects (http://www.insectgenome.com/). The accession numbers of sequences are
given in Table S1.
Amino acid sequences were aligned with the program
MUSCLE [15], and the alignment was manually curated for
uncertainties and then served for building a maximum
likelihood tree using the server Phylogeny.fr (http://www.
phylogeny.fr/), with default parameters [16].
3 Results
3.1 Occurrence of the AHA-like C-terminal
domain in Bacteria
The C-terminal domain, around 185 amino acids
in length, was found only in a limited set of
γ-proteobacteria, mostly Alteromonadales, for instance
Pseudoalteromonas atlantica (YP_662421) and a number
of closely related species, e.g. P. tunicata (ZP_01134110)
and Alteromonadales bacterium TW7 (ZP_01613200),
all attached to an α-amylase orthologous of that of P.
haloplanktis (subfamily GH13_32 in the classification of
Stam et al. [17]). It was also found in two Cellvibrionaceae
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28 Jean-Luc Da Lage
– first in Saccharophagus degradans; it had been found
previously linked to a plant-type (subfamily GH13_6) [12].
We found a gene orthologous to this plant-type gene,
also with the C-terminal domain, in Cellvibrio japonicus
(ACE84223). Moreover, in this species, we also found a
duplicate of the C-terminal domain in C-terminal position
of the protein aqualysin (ACE84702). The Alteromonadales
Thalassomonas actiniarum (WP_044836227) and another
γ-proteobacterium
(Chromatiales),
Rheinheimera
nanhaiensis, were found to have a C-terminal domain,
attached to a plant-type amylase (WP_008218869). We
found no other occurrence among thousands of bacterial
genomes available at the NCBI, although the GH13_32
α-amylase type (i.e. the most related to the animal types)
occurs in a few dozens of various bacterial species, not
only γ-proteobacteria [13].
3.2 Occurrence of the AHA-like C-terminal
domain in metazoans
We searched the domain in genome databases, but also
experimentally for several non-vertebrate species. The
results are summarized on a species tree (Fig. 1). As a
whole, we found sequences similar to the AHA C-terminal
domain in various Protostomes and Deuterostomes. It
was found in non-hexapod pancrustacea, in nematodes,
molluscs, annelids, echinoderms and cephalochordates,
but not in insects, myriapods, arachnids, urochordates
and vertebrates. Like in bacteria, the length of the
domain was around 185-190 residues. In some cases,
when the domain was detected, there was no evidence for
its attachment to the catalytic part of α-amylase. It was
the case with some EST databases, where no sequence
was evidenced to show a continuity between the two
parts of the protein. Interestingly, as we will see below,
the C-terminal domain may exist independently from
an amylase. In several cases, two types of α-amylase
genes were found, with or without a C-terminal domain
(Fig. 1). Note that no α-amylase gene at all was found
in sequenced genomes of Platyhelminthes (Schmidtea
mediterranea, Schistosoma mansoni), of the leech
Helobdella robusta, of the aphid Acyrthosiphon pisum
and of the louse Pediculus humanus. Our results clearly
demonstrate that the AHA-like C-terminal domain was
already present in the ancestor of all extant Bilateria.
Indeed, one intron position is conserved across
Protostomes and Deuterostomes (Fig. 2). It is not quite
clear whether, at the time of the last bilaterian ancestor,
two types of genes already existed, or if the domain
was specifically lost independently a number of times
following gene duplications. The evolutionary history of
animal α-amylases is quite complex, because numerous
independent gene duplications and sequence divergences
occurred, so that a tree drawn from these sequences does
not faithfully reflect animal phylogeny (for instance,
nematode sequences are highly divergent, whereas
these organisms should be clustered with arthropods).
However, when reported on such an α-amylase gene tree
(Fig. S1), the presence of the additional domain seems to
be distributed along two main branches (which may reflect
a very old duplication), but with much more occurrences
in one of the branches. Some molluscs and crustacea
have sequences in each main branch, some with the
C-terminal domain, some being domainless. The domain
thus seems to have been lost several times independently,
and completely at least in Vertebrates + Tunicates and in
insects. In the latter cases, data are yet too scarce to clarify
its presence or absence in early diverging Hexapoda, such
as Collembola, which would help to date the loss event
in insects. Genomes and individual sequences available
to date in databases, such as GenBank, Flybase (http://
flybase.org/) or InsectBase (http://www.insect-genome.
com/) do not exhibit the C-terminal domain. For the
same reason, we cannot conclude firmly to a complete
loss in the clade of Myriapoda + Chelicerates, although
complete amylase genes lacking the C-terminal domain
have been sequenced. The former characterization of
only C-terminal domainless α-amylases in some molluscs
or crustacea, generally from mRNAs [18-20], suggested
that these C-terminal domainless genes were the most
active ones. However, EST libraries showed that the
α-amylases linked to the AHA-like C-terminal domain
may be transcribed as well.
3.3 The Daphnia pulex case
Independent losses of the C-terminal domain may indeed
occur, as illustrated by the situation in the genome of
Daphnia pulex (Crustacea, Branchiopoda). In this species,
there are at least four α-amylase gene copies, two of which,
Amy1 and Amy1’ are tandem duplicates. The duplication
has involved about 500 bp upstream of the start codon
and all the usual coding sequence of an α-amylase.
Sequence identity is almost complete in the second half
part of the gene, probably due to gene conversion (Fig. S2).
And yet, Amy1 has a C-terminal domain, whereas Amy1’
has not. It is likely that the domain was lost in Amy1’
during the duplication event, as the duplicated segment
stopped inside the linker. It is unlikely that the domain
was gained in Amy1 (e.g. from Amy2), since the tree of
C-terminal domains (Fig. 3) shows no closer relationship
of the C-terminal domain between Amy1 and Amy2.
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C-terminal α-amylase domain in animals
29
Figure 1. Animal species tree (consensus from the literature [27-33]) showing the occurrences of the optional C-terminal domain. Legend:
“+”, domain present; “-”, domain absent; “+ & -”, occurrence of both gene copies with and without the domain; (1), no evidence of attachment to α-amylase; (2), very long subterminal intron inside domain C.
3.4 Origin of the linker region
The C-terminal domain has always been found to be
linked to the enzyme by a low-complexity linker about
20-50 residues in length (shorter in Nematodes), often rich
in proline, threonine, serine and glycine. We defined the
linker region by the amino acid sequence lying between
the end of the usual, conserved α-amylase sequence,
that is, the end of domain C succeeding the TIM barrel,
and the first conserved stretch RTVIF in the C-terminal
domain. In the species studied, the linkers were highly
variable in sequence, compared to both the core enzyme
sequence and the C-terminal domain. Functionally, the
biased amino acid composition of the linkers endows
them with properties typical of linkers joining catalytic
domains and CBMs in various glycoside hydrolases. We
studied specifically the linkers and their mechanistic
dynamics elsewhere [21]. Although we have shown that
the C-terminal domain is ancestral, it might have moved or
been duplicated from one copy to another, as it happened
in the bacterium S. degradans. If some C-terminal domains
have been recruited by previously domainless α-amylase
genes through exon shuffling, what would be the origin of
the amino acid linkers? In some species, the gene region
encoding the linker contained an intron (amphioxus AmyA
and AmyB, Daphnia Amy2). In the Annelide Capitella
teleta and all the molluscs, the linker was preceded by an
intron, subterminal relative to the usual enzyme sequence
[22]. However, there is no indication in our sequence
analyses for partial or complete exonisation of introns,
nor internal duplications, which could have mediated the
building of independent linker regions. One may notice
in amphioxus AmyA a fourfold repeat of His-Pro-Thr.
This motif, and other ones, such as poly-Thr (Capitella),
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30 Jean-Luc Da Lage
Figure 2. Alignment of C-terminal domains of bacteria and animals, truncated to the most commonly found end. Colours show similarities as
follows: red, 100% similarity; orange, 80-100% similarity; yellow, 60-80% similarity; white, below 60% similarity. Intron positions, when
known, are indicated by vertical bars: pink, phase 0; blue, phase 1; green, phase 2.
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poly-Gly (sea urchin) may stem from three-nucleotide
microsatellites. At least this kind of mechanism may have
shaped very dissimilar linker regions, whatever their
common or independent origins. On the other hand, the
linker region may enhance the probability of loss of the
C-terminal domain, as shown in Daphnia genes, where
the deletion breakpoint seems to have occurred within
the linker, since a part of the linker remains at the end of
Amy1’ (Fig. S2). The same remark could also apply to the
C-terminal α-amylase domain in animals
31
scallop Pecten maximus, the oyster Crassostrea gigas and
the abalone Haliotis discus – genes devoid of C-terminal
domain have been characterized in these species (P91778,
AF321515, EF103352) – but careful examination shows
that they expand a bit downstream of the usual end of the
enzyme (end of the domain C), suggesting the presence of
a relictual part of a linker, and thus a loss of the C-terminal
domain. We have done a similar observation in sea urchin
α-amylases (XP_011683732, XP_782889 and XP_794418).
Figure 3. Tree drawn from the alignment of C-terminal domains of bacteria and animals. Colour legend: orange, bacteria; pink, crustacea;
blue, molluscs; green, nematodes; red, deuterostomes. Figures along branches are the posterior probabilities of the maximum likelihood
computation.
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32 Jean-Luc Da Lage
3.5 Analysis of the alignment
The alignment of C-terminal domains of bacteria
and animals (Fig. 2) shows that the sequences are
characterized by the presence of four highly conserved
cysteines in bacteria, with two more cysteines in animals.
At positions 107-114 of the alignment, a deletion occurred
in Protostomes. In silico predictions (http://clavius.
bc.edu/~clotelab/DiANNA/) suggest that two or three
disulphide bonds, respectively, may be formed, although
with moderate confidence. As already noticed for AHA
[10], the predicted secondary structure is dominated by
β-strands (http://www.compbio.dundee.ac.uk/jpred/). De
novo structure predictions are not satisfactory. The CABSFOLD server (http://biocomp.chem.uw.edu.pl/CABSfold/)
proposed several structures, the preferred of which showed
a very flat sheet shape, which is not consistent with the
predicted secondary structures (not shown). The QUARK
server (http://zhanglab.ccmb.med.umich.edu/QUARK/;
[23]) showed a structure, which is more consistent with
the secondary structure predictions, but it did not predict
disulphide bonds (Fig. 4). In addition, iTASSER (http://
zhanglab.ccmb.med.umich.edu/I-TASSER/)
predicted,
with low confidence, the presence of an acarbose binding
site for both C. fluminea and AHA, and also a maltose
binding site for AHA (not shown).
3.6 Occurrences of the C-terminal domain,
not linked to an α-amylase
In the bacterium Cellvibrio japonicus, we found an AHAlike C-terminal domain linked to a non-amylase enzyme,
the aqualysin, an extracellular serine protease. This
enzyme has been described in few bacteria, and possesses
both N-terminal and C-terminal propeptides involved
in extracellular translocation [24]. However, those
domains have no relationship with the additional AHAlike C-terminal domain found in C. japonicus. Although
this case of domain shuffling most likely stems from a
duplication of the α-amylase C-terminal domain, the tree
(Fig. 3) shows a rather fast divergence with its parent
domain.
In animals, we found cases of duplicates of the
C-terminal domain independent from α-amylase in
Daphnia pulex only. Three occurrences were detected in
the genome (http://wfleabase.org/): (i) on the scaffold 14
(JGI_V11_100284, nuc. 1142036-1144649); (ii) scaffold 51
(JGI_V11_323078, nuc. 789341-790623); and (iii) scaffold
183, (JGI_V11_229423, nuc. 111544-112544). The latter of
those duplicates was physically close (ca. 7 kb apart) to
the α-amylase gene Amy2, which contains a C-terminal
domain. However, the sequences of the three duplicates
were clustered together rather than with a putative
α-amylase donor (Fig. 3), which suggests a common
origin of these three domains, their ancestor having
already diverged significantly from the Amy counterparts.
However, the three sequences nonetheless shared the same
intron positions as the sequences of C-terminal domains
linked to α-amylases (Fig. 2). All of these duplicates were
predicted to be linked to putative polypeptides with a
linker-like sequence, but the reality of such neogenes
was not ascertained. ESTs suggested transcription for
the putative genes on scaffold 183 (WFes0162386) and
51 (Wfes0148654), but there were slight differences
between the ESTs and the genomic sequences, and, more
importantly, a lack of the protein parts predicted to be
upstream of the linkers. In addition, the putative genes
linked to an AHA-like C-terminal domain in scaffolds 14
and 51 shared similarities in their N-terminal part. This
part, in turn, seems to be present in several copies in the
Daphnia genome (eight hits in a BLASTP search).
4 Discussion
Figure 4. De novo three-dimensional model of the C-terminal domain
of Corbicula fluminea obtained with the QUARK server [23] and
drawn with the Swiss-PdbViewer [34].
We have shown here that an extra protein domain,
linked in C-terminal position to the domain C of animal
α-amylases, is widespread in bilaterian animals. Indeed,
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it has long remained unnoticed because the most
studied animal α-amylases were those of mammals
and insects, which both lack this domain. We call it an
optional domain also because, even in species where it is
found, it may be present or absent if several gene copies
occur, which is quite common. The domain is ancestral
in bilaterian animals and may have accompanied the
transfer of a bacterial amylase to a bilaterian ancestor [13].
Interestingly, only a small number of bacteria possess this
domain and are eligible for a donor status. It is possible
that the donor was a symbiont, since horizontal gene
transfer from symbiotic bacteria to their hosts has been
often reported, endowing the receptor organism with new
abilities, and rendering it independent from its symbiont
[25]. Another noteworthy fact is that the C-terminal
domain, although not frequently, has been recruited by
other genes, in bacteria as well as in animals (in Daphnia,
namely). The presence of a linker or an intron between
the core sequence and the terminal domain increases
the likelihood of exon or domain shuffling. But for what
function? No interaction of the AHA C-terminal domain
with insoluble polysaccharides was noticed (Georges
Feller, Université de Liège, personal communication).
The sequence of the domain is quite different from that
of SBDs or other CBMs, except that it shows a structure
that is rich in β-sheets. The β-sheet-rich structure was
confirmed in AHA using infra-red spectroscopy, but
this experimental method also retrieved 29% helices,
which is not proposed by in vitro modelling. In addition,
two disulphide bonds were found experimentally [26].
In P. haloplanktis, where it was first described and
best characterized, it has been proposed to serve as a
“secretion helper” for export across the periplasmic
membrane of bacteria [10], but this hypothesis remains
debatable because it also occurs in animals. In animals,
it might be used as an anchor to cell membranes, but not
through transmembrane anchoring, since it shows no
transmembrane domains (http://www.ch.embnet.org/
software/TMPRED_form.html). However, to date, we do
not know whether, in animals, the C-terminal domain
remains attached to the core enzyme or if it is cleaved like
in AHA. In vitro experiments using an antibody raised
against the AHA “propeptide”[10] on mussel or daphnia
extracts on Western blots gave unclear results, because
although the antibody would react well with animal
domains, it seems that artifactual cleavages occurred,
making interpretations difficult (not shown). Further
studies are needed to assess the in situ localization of
the C-terminal domain in animal tissues and its possible
co-localization with the core enzyme.
C-terminal α-amylase domain in animals
33
Acknowledgments: I am grateful to Georges Feller for
fruitful advice and discussion. The work was funded by
regular CNRS funding to my laboratory.
Conflict of interest: The author declares no conflict of
interest.
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