News date: 9.1.2017
compiled by Dr. Alvarinho J. Luis
Newly discovered phytoplankton groups
appear to favor warmer oceans
Summary: An international research team has discovered two phytoplankton
groups -- unlike any known species -- in climate-sensitive areas around the
world. While they appear relatively rare compared to other phytoplankton,
scientists say their prevalence in warm waters suggests they could be important
in future ocean ecosystems.
The study traced the phytoplankton genes to their potential ancient origins and matched them
with sequences in around 200 contemporary samples. The new phytoplankton groups were
increasingly abundant in warmer, low-nutrient surface waters at sites including the Sargasso Sea,
Bay of Bengal and North Pacific Gyre.
These new phytoplankton appear to thrive in the world's most desert-like waters where most
other eukaryotic species decrease, said Alexandra Z. Worden, who led the team from the
Monterey Bay Aquarium Research Institute (USA) alongside collaborators from Oregon State
University (USA), WHOI (USA) and the NIO (India).
Both phytoplankton groups were found in larger numbers in warmer, low-nutrient surface waters
compared to numbers in cooler, higher-nutrient regions. This pattern surprised researchers
because larger, eukaryotic phytoplankton often decline to vanishingly-low numbers under these
conditions, which typically favour small cyanobacteria.
Ocean surface warming creates a layer of low-nutrient water separate from cooler, nutrient-rich
water below. This process occurs annually in large regions of the open ocean where punctuated
winter mixing allows for a short "bloom" of phytoplankton life that is followed by a summer
season of warm, low-nutrient surface waters. Most of the bloom species disappear during
summer because they are not effective competitors for nutrients at low concentrations. Ocean
surface warming is leading to an expansion of these low-nutrient environments in a process
known as ocean desertification.
Scientists have had difficulty measuring the impact of ocean warming on resident microbial
groups due to a lack of consistent information on microbes, like the phytoplankton that carry out
marine photosynthesis. Worden's team established the Baselines Initiative to overcome this
hurdle with more than 6000 full-length RNA sequences and time-series sampling, where the
same location is sampled repeatedly through the seasons and over the years. The ultimate goal of
these oceanographic time-series is to capture current day information against which future
changes in the ocean can be assessed.
Researchers first discovered one of the new phytoplankton groups in 2006 when they noticed
one "weird" sequence out of millions. They thought the data from a tropical island off Costa Rica
might have been a mistake until they saw identical sequences in the North Pacific and in coral
reefs off Curaçao. To verify their findings, they filtered the organisms' DNA from the seawater.
Next, they generated the full-length RNA gene sequence and compared it with other organisms
to place it in an evolutionary tree. Finally, they mapped the organisms through samples from the
BIOS Bermuda Atlantic Time-Series Study, the TARA Oceans Expedition and the Baselines
Initiative, including the SeaFar Curaçao project of the Integrated Microbial Biodiversity
Program.
The first phytoplankton lineage appears to be an entirely new group of species of phytoplankton.
Researchers believe its ancestor may be a single-celled protistan group that took a separate
evolutionary path from the haptophyte algae, which arose between 1 billion and 637 million
years ago. The second lineage appears to be closely related to haptophytes. However, it is a new
group that doesn't belong to any known species or class.
There is a need to better understand the ecology of the two phytoplankton groups. How these
groups contribute to the food chain and carbon cycle is currently unknown. One possibility is
that they get their nutrients though a combination of photosynthesis and feeding on other cells.
Further research is required in this direction……
Journal Reference: Chang Jae Choi, Charles Bachy, Gualtiero Spiro Jaeger, Camille Poirier, Lisa
Sudek, V.V.S.S. Sarma, Amala Mahadevan, Stephen J. Giovannoni and Alexandra Z. Worden.
Newly discovered deep-branching marine plastid lineages are numerically rare but globally
distributed. Current Biology, 2017 DOI: 10.1016/j.cub.2016.11.032
Source: Canadian Institute for Advanced Research
Pdf reprint follows……
Current Biology
Magazine
A
Viridiplantae
0.96/
72/80
S1
DPL1, DPL2
Bay of Bengal % Plastids
Stramenopiles
EF574856
CN207-155S3Ab030
0.92/
50/80
DPL2
Haptophytes (Pavlovophyceae)
Rappemonads
CN207-155S3Ac8La
C0912-2
(1/2)
10˚N
0.2 1.0 2.0
80˚E
D
85˚E
90˚E
0
BATS
25
DPL1
100
Depth (m)
1/89/97
Haptophytes
(Prymnesiophyceae)
30
20
15
0.5
0.4
0.3
0.2
0.1
0
200
0
100
0.2
200
3
B
Chl ɑ (µg L-1)
Ocean surface warming is resulting in
an expansion of stratified, low-nutrient
environments, a process referred to as
ocean desertification [1]. A challenge for
assessing the impact of these changes
is the lack of robust baseline information
on the biological communities that
carry out marine photosynthesis.
Phytoplankton perform half of global
biological CO2 uptake, fuel marine food
chains, and include diverse eukaryotic
algae that have photosynthetic
organelles (plastids) acquired through
multiple evolutionary events [1–3]. While
amassing data from ocean ecosystems
for the Baselines Initiative (6,177 near
full-length 16S rRNA gene sequences
and 9.4 million high-quality 16S V1-V2
amplicons) we identified two deepbranching plastid lineages based on
16S rRNA gene data. The two lineages
have global distributions, but do not
correspond to known phytoplankton.
How the newly discovered
phytoplankton lineages contribute to
food chains and vertical carbon export
to the deep sea remains unknown,
but their prevalence in expanding, low
nutrient surface waters suggests they
will have a role in future oceans.
Phylogenetic relationships between
the two deep-branching plastid
lineages and other phytoplankton were
established using an alignment of
near full-length 16S rRNA genes that
incorporated new plastid sequences
from Baselines (see Supplemental
Information, published with this article
online). These were generated from three
North Pacific sites to augment the SILVA
database. The general relationships
15˚N
ARLs
(1/2)
S18
India
Cryptophytes
Red algae
1/65/92
1/60/90
1,6
Chang Jae Choi , Charles Bachy ,
Gualtiero Spiro Jaeger2,
Camille Poirier1, Lisa Sudek1,
V.V.S.S. Sarma3, Amala Mahadevan2,
Stephen J. Giovannoni4,
and Alexandra Z. Worden1,5,*
20˚N
1/65/55
DPL1
2
BATS
Bay of
Bengal
1
0
3
DPL2
2
1
Baselines Initiative
DPL1 Only
DPL2 Only
Both DPL1 & 2
Tara
1,6
Glaucophytes
Temp (°C)
Newly discovered
deep-branching
marine plastid
lineages are
numerically rare but
globally distributed
C
Cyanobacteria
% Plastids
Correspondence
0
-1 DM +1 +2 +3 +4 +5 +6 +7 +8 +9 +10
Time (month from Deep Mixing, DM)
Figure 1. Phylogeny and distribution of the novel deep-branching plastid lineages (DPLs).
(A) Reconstruction of plastid 16S rRNA gene sequences illustrating the positions of DPL1 (orange)
and DPL2 (blue). Apicomplexan-Related-Lineages (ARLs) and DPL1 branch-lengths are reduced
by 50% and the tree is rooted for display purposes; cyanobacteria are the outgroup. Posterior
probability/RAxML/PhyML bootstrap percentages are shown when >0.9/50/50 or fully supported
in all analyses (black dots). (B) DPL detection in Baselines 16S rRNA V1-V2 amplicon data from
non-size fractionated surface samples (closed circles) in the North Pacific (6 samples), Indian
Ocean (29), near Curaçao (14) and Sargasso Sea (85 BATS samples), and in Tara Oceans photiczone 16S miTAGs (<200 m depth; open circles). The 77 Tara 0.2 to <3 µm size-fraction photiczone samples with DPL1 (n = 32, 22.2 ± 5.5oC) and/or DPL2 (n = 50, 22.1 ± 3.8oC) were warmer
than those where not detected (17.6 ± 8.4oC, p < 0.05). (C) DPL1 (orange) and DPL2 (blue) percent
contributions to Indian Ocean 16S plastid amplicons. (D) Temperature and phytoplankton-derived
chlorophyll a concentrations (top two plots) show BATS seasonal changes. The X-axis reflects a
seasonal composite of 12 years of monthly data [8] adjusted to timing of deep mixing (DM) and
months post or prior to DM (numbers). Mean percent DPL1 or DPL2 (± standard error) in plastidderived 16S amplicons (bottom plots) highlights dynamics in BATS surface samples (0.3 to 7.6 m).
Samples from winter (21oC; typically –1, DM and +1) had lower relative abundances than during
stratification (p < 0.01).
illustrated were consistent with prior
studies [3–5]. Glaucophytes, Viridiplantae
and Red Algae, which arose from the
primary endosymbiosis event, emerged
in the basal region of the tree while
important marine taxa that arose from
secondary (or higher level) events, such
as haptophytes and stramenopiles [3],
formed distinct clades elsewhere (Figure
1A). The novel plastid lineage referred to
here as deep-branching plastid lineage 1
(DPL1) was discovered in samples from
the edge of the North Pacific Gyre (NPG)
and coastal California. Complete DPL1
16S rRNA gene sequences acquired
by two PCR approaches had best
blastn hits of 85% nucleotide identity
to unascribed environmental clones in
GenBank (Supplemental Information).
In phylogenetic reconstructions, DPL1
branched adjacent to haptophytes
(Prymnesiophyceae), albeit with
long branch-lengths (Figure 1A).
Testing of phylogenies using varied
taxonomic sampling established that
DPL1 sequences do not come from
dinoflagellates (at least not those
with available molecular data). When
fast-evolving dinoflagellate plastid
sequences with known haptophyte
origins [6] were included, DPL1
branched in unsupported or weakly
supported positions adjacent to the
Prymnesiophyceae and sister to the
Current Biology 27, R1–R18, January 9, 2017 © 2017 The Author(s). Published by Elsevier Ltd. R15
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Current Biology
Magazine
dinoflagellate plastids, or within the
Prymnesiophyceae (Figure S1A,B).
Diversity of DPL1 (DPL1-clusters C, D,
and E) and phylogenetically related
novel amplicons (DPL1-related clusters
A, B, F–J) was manifested in the 16S
V2 variable region (Figure S1C–S1D).
DPL1 was present in a Baselines 3 µm
size-fractionated sample and nearly
all non-fractionated samples, but not
picoplankton (<3 µm) samples. Thus,
we postulate DPL1 sequences originate
from a diverse eukaryotic protistan
group, with cells 3 µm diameter, that
bears tertiary plastids of haptophyte
origin.
Another plastid lineage unrelated
to known phytoplankton, ‘DPL2’, was
recovered from the picoplankton size
fraction in oligotrophic NPG waters.
They exhibited 99.6% nucleotide identity
to a clone from surface waters near
Costa Rica (GOS site 25), a Pacific
Ocean site with higher temperature
(28.3oC) and lower salinity (31.4 ppt) than
our NPG site (19.0oC, 33.2 ppt). DPL2
sequences branched in a sister position
to haptophytes, rappemonads and
DPL1 with moderate to strong bootstrap
support, suggesting they are derived
from secondary plastids (Figure 1A).
Analyses of molecular data alongside
fossil records indicate haptophytes arose
1,031–637 million years ago and that the
two haptophyte classes diverged 823–
328 million years ago [7]. This context
indicates an ancient origin of DPL2.
Global distributions of DPL1 and
DPL2 were mapped using Baselines
16S amplicon datasets from the North
Pacific, Caribbean (near Curaçao),
Sargasso Sea (at the Bermuda Atlantic
Time-series Study, BATS) and northern
Indian Ocean (Bay of Bengal), as well
as 16S rRNA gene fragments from Tara
Oceans (Table S1). Both novel lineages
were broadly distributed but not present
in colder Tara samples, and DPL2 was
found at more locations (Figure 1B). In
Baselines, DPL2 was also in mangrove
and saline pond samples from Curaçao,
while DPL1 was not. Wherever detected,
the newly identified lineages comprised
a small percentage of plastid amplicons,
0.93 ± 1.36% (DPL1) and 0.65 ± 0.63%
(DPL2), demonstrating these putatively
photosynthetic taxa are globally
distributed but often numerically rare.
For insight into DPL ecology, we
studied warm water environments,
where the surface is thermally stratified
R16
(BATS) and fresh-water stratified
(Bay of Bengal, Indian Ocean). While
detected in most Indian Ocean
samples, DPL1 (0.39 ± 0.43%, 24
stations) and DPL2 (0.38 ± 0.25%,
28 stations) contributions to plastidderived amplicons were low (Figure
1C), and trends with environmental
parameters unclear. However, at BATS
the new lineages exhibited their highest
individual sample contributions (10%
DPL1; 4% DPL2) to plastid counts
and pronounced seasonality. DPL1
and DPL2 contributed higher plastid
percentages during stratification than
during the winter period (Figure 1D)
when deep-mixing (>200 m) brings
nutrients from depth into the photic
zone and induces phytoplankton
blooms [8]. This trend persisted for
DPL1 groups when computed against
total amplicons (including bacteria),
akin to patterns for the oligotrophic
cyanobacterium Prochlorococcus [9].
When Prochlorococcus contributed
>10% of total 16S amplicons,
temperature (23.92 ± 2.68oC) was not
statistically different from samples
with highest DPL1/DPL1-related
contributions (Figure S1E–S1F).
However, DPL1/DPL1-related
contributions were lower (p < 0.001)
when eukaryotic phytoplankton as
a whole contributed >10% of total
amplicons, during which it was also
cooler (20.38 ± 0.89oC, p < 0.001) and
less stratified. This contrast suggests
that among eukaryotes at BATS [8]
DPL1/DPL1-related taxa may be
relatively effective competitors for
macronutrients.
Recent studies highlight previously
unrecognized sequence diversity within
known marine eukaryote classes. Our
discoveries are exceptional in identifying
new, deep-branching phytoplankton
lineages. Only two other such deepbranching uncultured plastid lineages
have been discovered in the last
decade: Rappemonads [5] and the
coral-associated Apicomplexan-RelatedLineages [4]. The distributions of the
lineages we discovered suggest they
tolerate a broad range of conditions,
but may increase numerically as ocean
warming progresses, akin to predictions
for Prochlorococcus [10]. The discovery
of the DPL algal groups in contemporary
samples illustrates the importance
of time-series sampling for acquiring
essential data points for comparison
Current Biology 27, R1–R18, January 9, 2017
as ocean ecology adjusts to changing
climate.
SUPPLEMENTAL INFORMATION
Supplemental Information contains
experimental procedures, one figure and one
table can be found with this article online at
http://dx.doi.org/10.1016/j.cub.2016.11.032.
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1
Monterey Bay Aquarium Research Institute,
Moss Landing, CA 95039, USA. 2Woods
Hole Oceanographic Institution, Woods
Hole, MA 02543, USA. 3National Institute
of Oceanography, Visakhapatnam, India.
4
Department of Microbiology, Oregon
State University, Corvallis, OR 97331, USA.
5
Integrated Microbial Biodiversity Program,
Canadian Institute for Advanced Research,
Toronto, Ontario M5G 1Z8, Canada.
6
Co-first authors.
*E-mail: [email protected]