A Hotspot of Amoebae Diversity: 8 New Naked Amoebae Associated with the Planktonic Bloom-forming Cyanobacterium Microcystis
Author
Van Wichelen, Jeroen
Author
D’Hondt, Sofie
Author
Claeys, Myriam
Author
Vyverman, Wim
Author
Berney, Cédric
Author
Bass, David
Author
Vanormelingen, Pieter
text
Acta Protozoologica
2016
55
2
61
87
https://www.mendeley.com/catalogue/b604c599-ed8a-3422-8096-249caaf4697e/
journal article
298905
10.4467/16890027AP.16.007.4942
54e2a24e-cf3d-47dd-8d52-1cbe13ebd253
1689-0027
12538714
Korotnevella
All the dactylopodial strains were placed in the genus
Korotnevella
, which appeared monophyletic with good bootstrap and posterior probability support (
Fig. 2A
). The
Microcystis
-associated
Korotnevella
strains fell into two lineages, containing two and five strains respectively, without representatives of known species.
P
-distances were 4.9–5.9% (75–99 differing positions) between both lineages and 0.0–1.7% (0–23) within a lineage.
Locomotive amoebae belonging to the first lineage, strains A4
DVDPB
and A1
JEPDK
, were triangular, elongated or irregularly shaped (
Fig. 2B
). No differentiated uroidal structures were observed. Feeding amoebae (on
Microcystis
colonies) were spherical to cylindrical without dactylopodia (
Fig. 2B
7
) but sometimes with a very long and thin sub-pseudopodium when maintained in starved conditions. Length of the locomotive form was 16–41 µm (mean 28), width 6–20 µm (11) and length/width ratio 1.2–6.0 (2.6). One vesicular globular nucleus about 2–3 µm in diameter was present containing one slightly eccentrically located globular nucleolus of about 1–2 µm, occasionally showing a highly refractive central pore-like area (lacuna) under phase-contrast illumination (arrow in
Fig. 2B
7
). Floating forms were spherical with a diameter of 10–16 µm (14) and displaying 4–10 long, hyaline, pointed pseudopodia of maximally 25 µm long. Large spherical planktonic aggregates of up to several hundred individuals were observed occasionally in older cultures. Cysts were never observed. The scales, covering the entire cell surface, consisted of an elliptical disc with upwards curved edges and a centrally located cone-like spine giving it a ‘witches hat’ appearance (
Fig. 3a, c
). The length of the scales observed at top view (
Fig. 3a
) varied from
193–327 nm
(277), the width from
124– 203 nm
(172) and the L/W ratio from 1.2–2.1 (1.6). The spine length observed in cross-section (
Fig. 3c
) was
47–97 nm
(76), width at the base
56–124 nm
(80) and L/W ratio 0.5–1.5 (1.0).
The locomotive amoebae from the second lineage, strains A8
WVB
,
A16
WVB
,
A21
WVB
,
A54
WVB
and A1
LMS
, were all triangular, elongated or irregularly shaped due to the formation of short to deeply inclined pseudopodia on one or both ends or all around the cell body (
Figs 2C
3
,
4
,
8
–12). No differentiated uroidal structures were observed. Amoebae during non-oriented movement were elongated (
Figs 2C 2
,
6
) or irregularly shaped (
Fig. 2C
1
), containing several small, sometimes bifurcated, round-tipped pseudopodia. Feeding amoebae (
on
Microcystis
colonies) were spherical to cylindrical without clear pseudopodia (
Fig. 2C
5
). Starved amoebae had a similar cell shape but sometimes contained a very long and thin sub-pseudopodium. Cell length during locomotion was 20–65 µm (mean 37), width 6–32 µm (14) and the length/ width ratio 1.2–6.0 (2.8). One vesicular globular nucleus about 6 µm in diameter was present containing one slightly eccentrically located globular nucleolus of about 3 µm (arrows in
Figs 2C
8
, 10, 12), occasionally showing a highly refractive central pore-like area (lacuna) under phase-contrast illumination (faintly visible in
Fig. 2C
8
). Floating forms (
Fig. 2C
13) were of radial
type
, spherical, with a diameter of 10–25 µm (15) and displaying 1–20 (9) long, hyaline, pointed pseudopodia with a length of 20–100 µm (52). The entire cell surface was covered with scales, only visible with electron microscopy (
Figs 3b, d
). In cross-section (
Fig. 3d
), these were generally oriented in a roof-tile pattern (imbricated). The scales consisted of an elliptical disk with upwards curved edges and a centrally located cone-like spine giving it a ‘witches hat’ appearance. The length of the scales observed at top view was
260–391 nm
(333), the width
153–206 nm
(180) and the length/width ratio 1.5–2.6 (1.9). The spine length measured on scales observed in cross-section was
98–163 nm
(121), the width measured at the base of the spine
61–131 nm
(91) and the length/width ratio 0.8–2.2 (1.4). Starved amoebae tended to float and aggregate into large, spherical colonies of several tens to hundreds of individuals. A few times, a globular cyst-like body with a diameter of 15– 20 µm was observed in the cultures (
Fig. 2C
7
)
.
Fig. 1. A
– 18S rDNA maximum likelihood phylogeny of
Vannella
, including
Microcystis
–associated strains (in bold). ML bootstrap values respectively posterior probabilities are shown at the nodes. GenBank accession numbers are given together with the species names.
B
– LM pictures of
V. planctonica
(strains A2FBB: 2, 4, 5, 9–13 and A4P4ZHB: 1, 3, 6–8) showing locomotive trophozoites (1–8), a grazing amoeba with a
Microcystis
cell inside a food vacuole (9), floating forms (10–11) and a cyst stage (12–13).
C
– LM pictures of
V. simplex
(strain A17WVB) showing the floating form (14), locomotive amoebae (15–18) with the presence of food vacuoles containing partly digested
Microcystis
cells (17), posteriorly adhered fecal pellets (15–16), a long flagellum-like pseudopodium encircling a
Microcystis
cell (17–18) and grazing amoebae on a colony of
Microcystis aeruginosa
with expanded (arrow) or contracted (arrowhead) flagellum-like pseudopodia visible in some of the trophozoites (19). The presence of a contracticle vacuole, a nucleus or a cyst opening is indicated by a black arrow, a black arrowhead or a white arrow respectively. Scale bars: 20 µm.
Korotnevella
is a genus of scale-bearing amoebae all characterized by the absence of parasomes (
Smirnov
et al
. 2011
). Currently 8
Korotnevella
species are recognized – 4 from freshwater, 3 from marine habitats and 1 from terrestrial origin – that are mainly distinguished on the base of their scale morphology (
O’Kelly
et al
. 2001
,
Udalov 2015
). The
Korotnevella
species without 18S rDNA sequence data are
K. nivo
, a marine species with crown-like scales (
Smirnov 1996
/97), 3 freshwater species, being
K. bulla
with basket-like scales (
Page 1981
),
K. diskophora
with disc-like scales (Smirnov 1999) and
K. limbata
having both scale
types
(
Udalov 2015
) and the terrestrial
K. heteracantha
also bearing both scale
types
(
Udalov 2015
). TEM analysis of the
Microcystis
-associated
Korotnevella
strains from both lineages showed the presence of disc-like scales (
Fig. 3
) very similar to the scales of
K. diskophora
. Apart from some small differences in scale dimensions and spine length, our strains mainly differed from
K. diskophora
, by having a spherical floating form with radially many pointed pseudopodia (irregular with few pseudopodia in
K. diskophora
) and by their preference for
Microcystis
and thus planktonic occurrence (bacterivore and benthic lifestyle in
K. diskophora
). Apart from the phylogenetic divergence, both
Microcystis
-associated
Korotnevella
lineages also differ in their morphology since the size of the trophozoites and of the scales and spines is smaller in strains of the first lineage (A4
DVDPB
and A1
JEPDK
). Based on the above-mentioned differences between both
Microcystis
-associated
Korotnevella
lineages and with
K. diskophora
,
we described both lineages as new species,
K. pelagolacustris
and
K. jeppesenii
.