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Bacterial associations with the hydromedusa Nemopsis bachei and scyphomedusa Aurelia aurita from the North Atlantic Ocean
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Bacterial associations with the hydromedusa
Nemopsis bachei and scyphomedusa Aurelia
aurita from the North Atlantic Ocean
Meaghan C. Daley, Juanita Urban-Rich & Pia H. Moisander
To cite this article: Meaghan C. Daley, Juanita Urban-Rich & Pia H. Moisander (2016): Bacterial
associations with the hydromedusa Nemopsis bachei and scyphomedusa Aurelia aurita from
the North Atlantic Ocean, Marine Biology Research, DOI: 10.1080/17451000.2016.1228974
To link to this article: http://dx.doi.org/10.1080/17451000.2016.1228974
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3. 1758), of the Cnidarian classes Hydrozoa and Scypho-
zoa, respectively, both collected from Western North
Atlantic coastal waters. Nemopsis bachei is a colonial,
relatively small species (up to 11 mm bell height),
with the polyp phase found in the Northern latitudes
between approximately 30°N and 60°N in both the
Atlantic and Pacific Oceans (Mendoza-Becerril &
Marques 2013), and the range extending to the Atlan-
tic Seashore and Gulf of Mexico (Marshalonis & Pinck-
ney 2007; Johnson & Allen 2012). Nemopsis bachei is
reported as native to the east coast of the United
States and the Gulf of Mexico (Moore 1958), and as
an invasive species in Northern European coastal
waters (Frost et al. 2010; Laakmann & Holst 2014). In
Chesapeake Bay in the Mid-Atlantic coast of the
United States, N. bachei has been noted as the most
important gelatinous predator of micro- and meso-
zooplankton during summer months (Purcell &
Nemazie 1992), and it was the most abundant hydro-
medusa in a South Carolina estuary (Marshalonis &
Pinckney 2007).
In contrast to the more geographically restricted,
potentially invasive N. bachei, A. aurita is cosmopolitan.
Aurelia aurita is larger than N. bachei (50–300 mm),
present in coastal waters and enclosed bays during
warm summer months, and feeds on micro- and meso-
zooplankton (Uye 2011). High abundances of A. aurita
have been shown to lead to decreased abundances
of herbivorous zooplankton and increased abundances
of phytoplankton and protozoa (Möller 1980; Feigen-
baum & Kelly 1984).
Cnidarians can have highly taxon-specific microbial
communities, reflecting a close interdependence of
the microbiome and the host in at least some species
(Bosch et al. 2015). In addition, environmental prefer-
ences and differences in food sources could promote
a distinct microbiome composition among invertebrate
host species (Tang et al. 2009). Differences have also
been reported even among subpopulations within
species, as well as among life stages and body parts
(Weiland-Bräuer et al. 2015). The goal of this study
was to characterize and contrast bacterial communities
associated with N. bachei and A. aurita, both of which
are a common part of the ecosystem in the temperate
coastal waters of the Atlantic Ocean, but could have
distinct microbial signatures, differentially influencing
the jellyfish ecophysiology or the ecosystem function.
The microbial communities in these jellyfish could
potentially reflect symbioses, an induced community
response, feeding interactions, or some combination
of these. Jellyfish could also potentially serve as
vectors or hosts of human or animal pathogens. This
may be the first published investigation of microbial
community composition in association with N. bachei,
and the first description of communities in A. aurita
in waters of the North-western Atlantic Ocean.
Materials and methods
Individuals of Nemopsis bachei (n = 15) were collected
from Mayflower Beach in Dennis, Massachusetts, USA
(41.744°N, 70.219°W) in 2–4 August 2012 (hereafter
’the Cape Cod site’). Specimens were collected at a
depth of 1 m by towing a hand net (34 cm in diameter,
2.5 mm mesh size) parallel to shore in 5 m transects.
Specimens collected from 10 tows were placed in con-
tainers holding 3 l of seawater, and seawater samples
were collected (n = 3) in acid-washed and combusted
IPEX or Wheaton bottles (Wheaton, Millville, NJ).
Samples were transported to the University of Massa-
chusetts Boston (UMB) within 3 h from collection.
Aurelia aurita samples (n = 7) were collected from
Boston Harbor on 12 and 22 May 2013. Specimens
were collected using buckets off two docks (42.311°N,
71.040°W and 42.293°N, 71.039°W) and placed in 3 l
of seawater. Samples for parallel seawater analysis for
A. aurita (n = 2) samples were collected similarly to
those for N. bachei. Boston Harbor samples of
A. aurita and parallel seawater were transported to
UMB within 1 h of collection.
In the lab the jellyfish individuals were transferred
from the seawater into 3 l of 0.2-µm filtered and auto-
claved artificial seawater (ASW) at local salinities (32
and 29 ppt for Cape Cod and Boston Harbor, respect-
ively). ASW was made using the manufacturer’s proto-
col (Instant Ocean, Blacksburg, VA). The jellyfish
remained in the ASW for approximately 2–3 h in
order for the animals to evacuate their guts, after
which they were then rinsed three times with the
ASW. Nemopsis bachei individuals were transferred
into autoclaved 2 ml bead beater tubes, then flash
frozen in liquid nitrogen. Aurelia aurita were dissected
using sterile scalpels and tweezers to select symmetri-
cal portions containing parts of the bell, cilia and tenta-
cles. The different parts from each individual were
combined into the same tube, then flash frozen as
above. All containers for collection and holding
animals were acid washed. Seawater (150 ml) from
each site was filtered through 0.2 μm Supor membrane
filters (Pall-Gelman, Port Washington, NY), which were
then placed in autoclaved 2 ml bead beater tubes
and flash frozen. All samples were stored at −80°C
until further processing.
DNA from seawater samples was extracted using a
MO BIO UltraClean Tissue & Cells DNA Isolation Kit
(Carlsbad, CA) using the manufacturer’s protocol.
2 M. C. DALEY ET AL.
4. Jellyfish samples were extracted using the same proto-
col, but the samples were homogenized before using
the kit protocol. The jellyfish samples were manually
ground for one minute using a sterile plastic pestle, fol-
lowed by the DNA extraction directly or after removal
of the largest jellyfish tissue particles. The large tissue
pieces were removed by filtration through a 2 µm poly-
carbonate filter (GE Osmonics, Greenville, SC) with
20 ml of nuclease free water, and the filtrate was
then collected and filtered on a 0.2 µm Supor filter,
which was used for DNA extraction. The microbial
16S rRNA gene was amplified from DNA extracted
from jellyfish and seawater samples using polymerase
chain reaction (PCR) primers 8F (5’-AGRGTTYGA-
TYMTGGCTCAG-3’) (Morris et al. 2004) and 519R (5’-
GWATTACCGCGGCKGCTG-3’) (Turner et al. 1999). PCR
reactions consisted of 1 μl each of the primers at
25 μM stock concentration, 5 μl 10× buffer, 2 μl 50-
mM MgCl2, 1 μl 10-mM dNTPs, 1 U (0.2 μl) Platinum
Taq (Invitrogen, Life Technologies, Carlsbad, CA), and
2 μl of template DNA. The reactions were adjusted to
50 μl with nuclease free water. The PCR consisted of
an initial denaturation at 95°C for 3 min, followed by
30 cycles of 94°C for 1 min, 55°C for 1 min, 72°C for 1
min and extension at 72°C for 7 min. Products were
separated on a 1.2% TAE agarose gel and visualized
with ethidium bromide. Bands were excised and gel
purified, then ligated into the pGEM-T vector, trans-
formed into competent E. coli JM109, and grown on
LB plates under ampicillin selection using the
manufacturer’s protocol (Promega, Madison, WI).
Sequencing was performed at the Massachusetts
General Hospital DNA Core Facility at Harvard Univer-
sity (Cambridge, MA), the sequences were trimmed
using CLC Main Workbench 6 (CLC Bio, Cambridge,
MA), and a chimera check was conducted using DECI-
PHER (Wright et al. 2012). Sequences were identified
using BLASTn and the RDP Classifier (Cole et al. 2009),
the latter based on an 80% threshold for phylum identi-
fication. The sequences were aligned using the online
SINA aligner (Pruesse et al. 2012) and imported into
the 16S rRNA SILVA database release 115 (Quast et al.
2013) in ARB (Ludwig et al. 2004) for creating neigh-
bour-joining phylogenetic trees. Bootstrapping was
performed in MEGA (version 5.2.2) with 1000 replicates.
The 16S rRNA sequences from this study are in
GenBank under accession numbers KP198297–
KP198503 (Table S1). Nemopsis bachei identification
was confirmed by conducting PCR targeting the mito-
chondrial cytochrome oxidase gene as previously
described (Folmer et al. 1994; Bucklin et al. 1999; Shoe-
maker & Moisander 2015). The COI sequence GenBank
accession numbers are KX265102–KX265109.
Statistical comparisons between bacterial commu-
nities were conducted (redundancy analysis and analy-
sis of variance) using R Studio. The sequence
abundances in different OTUs were standardized to
proportion of all sequences. The Euclidian distance
was used to compare operational taxonomic unit
(OTU, 97% DNA identity) presence and abundance
based on Hellinger transformed per cent composition
OTU data (Legendre & Gallagher 2001). An ordination
plot was created using a redundancy analysis (RDA),
with the constrained eigenvalues representing the
sample type (jellyfish or seawater) and location
(Boston Harbor or Cape Cod). Analysis of variance
(ANOVA) was performed on the RDA to test for differ-
ences in bacterial communities among the samples.
The ANOVA tests were run with 999 permutations
and P < 0.05 was considered significant.
Results
In the initial PCR reactions to amplify microbial 16S
rRNA, the high abundance of jellyfish DNA in the
samples resulted in strong amplification of the 18S
rRNA gene from the jellyfish. In subsequent DNA
extractions, the majority of the homogenized jellyfish
tissue was removed through a 2 µm filter and the fil-
trate used for DNA extraction and PCR (see Methods).
In most subsequent PCR reactions, bands for both
18S rRNA and 16S rRNA were observed, but using posi-
tive controls for each, the two bands could be
Figure 1. Per cent composition of bacterial phyla associated
with Cape Cod seawater (three samples, total of 61 sequences),
Nemopsis bachei (15 individuals, total of 92 sequences), Boston
seawater (two samples, total of 41 sequences) and Aurelia
aurita (seven individuals, total of 51 sequences) based on
RDP classifier results on 90% similarity.
MARINE BIOLOGY RESEARCH 3
5. distinguished in gel electrophoresis and 16S rRNA
bands selectively excised, cloned and sequenced
(Figure S1, supplementary material). A total of 245
sequences were recovered, of which 207 were
unique. A total of 74 and 43 unique sequences were
recovered from Nemopsis bachei and Aurelia aurita,
respectively, and 50 and 40 unique sequences were
recovered from the seawater collected in parallel with
N. bachei (Cape Cod seawater) and A. aurita (Boston
Harbor), respectively. All of the COI sequences from
the individuals morphologically identified as N. bachei
had a 99% nucleotide identity with N. bachei
(sampled from the North Sea, GenBank accession
KC440112.1).
Microbial community in Nemopsis bachei and
the Cape Cod seawater
Gammaproteobacterial sequences formed a total of
45% and 7% of Nemopsis bachei and Cape Cod sea-
water sequences, respectively (Figure 1). Vibrionales
were the most abundant Gammaproteobacteria in
N. bachei, forming 35% of all sequences. Sequences
from Oceanospirillales, Enterobacteriales, Alteromona-
dales and Vibrionales were all found in association
with N. bachei but not in Cape Cod seawater (Figure
2). The majority of the Vibrionales sequences from
N. bachei clustered with Vibrio spp., and one cluster
of sequences within Vibrionales was closely related
with Photobacterium swingsii (HE584802, 99% identity).
A cluster of Enterobacteriaceae sequences from
N. bachei was closely related with Shigella flexneri
(ADUV01000046, 97–99% identity).
Sequences from both N. bachei and the surrounding
seawater contained Alphaproteobacteria (20% of
N. bachei sequences and 10% of Cape Cod seawater
sequences) but were from different groups in N. bachei
and in the seawater. The majority of alphaproteobacter-
ial sequences from N. bachei grouped with Rickettsiales
(AF206298 Ehrlichia sp. 91–92% identity and U12457
Neorickettsia helminthoeca 90–91% identity) (Figure 2),
while one sequence grouped with Rhizobiales
(NR_117855, Devoisa glacialis 99% identity). In contrast,
Rhodospirillaceae and Rhodobacteraceae (Alphaproteo-
bacteria) sequences were recovered from the Cape Cod
seawater samples but not from N. bachei. Betaproteo-
bacteria formed 7% of Cape Cod seawater sequences
but were not found in N. bachei (Figure 1).
Bacteroidetes represented 8% of the sequences
from N. bachei but they were not obtained from the
parallel seawater (Figures 1 and 3). Of the total of 92
sequences from N. bachei, three sequences had a
94% identity with Polaribacter sp. (HM010403), one
had a 99% identity with Tenacibaculum mesophilum
(AB681059), and one had a 96% identity with Psychro-
serpens damuponensis (NR_109097), all within
Flavobacteriales.
Sequences from cyanobacteria or chloroplasts
formed 52% of all sequences from the Cape Cod sea-
water and 24% of sequences from N. bachei (Figures
1 and 3). The majority of them were within the clade
GpIIa that encompasses the picocyanobacteria Syn-
echococcus and Prochlorococcus (HM057705 and
GU170756, 98–100% identity). One of the phylotypes,
closely related to Synechococcus WH 8102, was
present in both N. bachei and the parallel seawater,
while two of the Synechococcus phylotypes (Synecho-
coccus CC9311 and CC9902) were present in the sea-
water only. An additional cyanobacterial sequence
was recovered from N. bachei clustering with the
non-heterocystous, filamentous cyanobacterium Lepto-
lyngbya sp. (JX481735, 97% identity).
Within Firmicutes, two sequences were recovered
from N. bachei but none were obtained from any
other sample types; these sequences had a high iden-
tity with Streptococcus salivarius (AB680535; 99% iden-
tity), falling in the Lactobacillales order (Figure 4).
Planctomycetes, Actinobacteria and Verrucomicrobia
represented 16%, 3% and 2% of the sequences in the
Cape Cod seawater (Figure 1) but were not found in
N. bachei. One N. bachei sequence had a 90%
identity with an uncultured Epsilonproteobacterium
(AB189341, isolated from a cold-seep). Of the
sequences from Cape Cod seawater, 3% were unclassi-
fied, with 98% identity to an uncultured marine bacter-
ium (HM225808) (Figure 1).
Microbial community in Aurelia aurita and the
Boston Harbor seawater
As in Nemopsis bachei, microbial communities from
Aurelia aurita and the parallel seawater were domi-
nated by different groups (Figure 1). Gammaproteo-
bacteria formed 6% and 2% of the sequences from
A. aurita and the corresponding seawater, respectively.
One gammaproteobacterial phylotype was recovered
from A. aurita, clustering with Psychrobacter immobilis
(U85880, 96–97% identity). In the Boston Harbor sea-
water, another gammaproteobacterial sequence type,
closely related with Vibrio sp. S3791 (FJ457558, 99%
identity), was present that was identical to sequences
from N. bachei sampled from the Cape Cod waters
further south (Figure 2). Alphaproteobacteria formed
22% of the community in the Boston Harbor seawater,
and a smaller proportion (4%) of sequences from
A. aurita (Figure 1). An alphaproteobacterial sequence
4 M. C. DALEY ET AL.
6. type within Rickettsiales was recovered from A. aurita
(Figure 2). Alphaproteobacterial sequences that were
not detected in any other sample type were recovered
from Boston Harbor seawater, including a sequence
from the SAR11 cluster, and sequences clustering
with Rhodobacteria.
Figure 2. Neighbour-joining tree of 16S rRNA sequences clustering with (a) Alphaproteobacteria and (b) Gammaproteobacteria.
Bootstrap values are shown where the value was 50% or higher based on 1000 permutations.
MARINE BIOLOGY RESEARCH 5
7. Flavobacteriales within Bacteroidetes were highly
represented in the Boston Harbor seawater. However,
Bacteroidetes formed only 2% of sequences in
A. aurita (99% identity with an uncultured Bacteroi-
detes/Chlorobi HQ242389 from the Northeast Pacific
seawater) (Figure 3). Cyanobacteria were detected in
both A. aurita and Boston Harbor seawater. All cyano-
bacterial sequences from A. aurita had the greatest
identity with cyanobacteria similar to the
Synechococcus CC9902 related phylotype obtained
from the Cape Cod seawater (Figure 3). The sequences
of this phylotype made up a large portion of all of the
sequences from A. aurita (35%). Chloroplast sequences
from Boston Harbor seawater accounted for 15% of
total sequences from this sample type and clustered
closely with uncultured Streptophyta (98% identity,
JF703621). Sequences clustering within the phylum
Tenericute of the class Mollicutes and order
Figure 3. Neighbour-joining tree of 16S rRNA sequences clustering with (a) Bacteroidetes and (b) Cyanobacteria. Bootstrap values
are shown where the value was 50% or higher based on 1000 permutations.
6 M. C. DALEY ET AL.
8. Mycoplasmatales were found at a high proportion
among A. aurita sequences but not in any other
sample type (Figure 4). Sequences distantly related to
Mycoplasma represented as much as 20% of the
sequences from A. aurita (84% identity with Myco-
plasma mobile strain NR_074620 and 85% identity
with an uncultured Mollicutes bacterium KC511181)
(Figure 4). Thirty-one per cent of the sequences in
A. aurita were distant (< 79% identity) to any classified
bacteria.
Microbial community in cnidarians vs. seawater
Rarefaction curves for Nemopsis bachei and Cape Cod
seawater had a similar slope, suggesting that the
level of richness recovered through sampling was
closely similar (Figure 5). Both jellyfish had lower diver-
sity than that of the surrounding seawater at the
phylum level, but at the OTU level, N. bachei diversity
was higher than that in the parallel seawater (Table I).
The microbial community composition of N. bachei
and that of Cape Cod seawater was significantly differ-
ent based on a one-way ANOVA on a redundancy
analysis (RDA) whether the analysis was conducted
by grouping the sequences by phylum (P = 0.048) or
OTU (P = 0.009) (Figure 6).
Rarefaction curves suggested that Aurelia aurita had
the lowest OTU richness of the four sample types
(Figure 5). The richness in Boston Harbor and Cape
Cod seawater was relatively similar, and similar to
N. bachei when comparing the curves at same sample
size as the seawater samples. Microbial communities
in A. aurita and Boston Harbor seawater were statisti-
cally different based on ANOVA and RDA analysis
whether the sequences were discriminated by
phylum (P = 0.045) or OTU (P = 0.049) (Figure 6). The
Figure 4. Neighbour-joining tree of 16S rRNA sequences clustering with Tenericutes, Firmicutes, Betaproteobacteria, Actinobac-
teria, Verrucomicrobia and Planctomycetes. Bootstrap values are shown where the value was 50% or higher based on 1000
permutations.
Figure 5. Rarefaction curves for the sequences recovered from
the different sample types based on 97% similarity. Number of
OTUs shown observed as a function of sample size in each
sample type (# of sequences). 1, Cape Cod seawater; 2,
Boston Harbor seawater; 3, Nemopsis bachei; 4, Aurelia aurita.
Table I. Shannon H diversity. Diversity calculated on the
number of sequences identified at OTU and phylum level
(OTU defined as 97% similarity).
#
samples
#
sequences
Shannon H
(OTU)
Shannon H
(phylum)
Nemopsis
bachei
15 92 3.66 1.46
Cape Cod
seawater
3 61 3.30 1.57
Aurelia aurita 7 51 2.92 1.57
Boston Harbor
seawater
2 41 3.20 1.64
MARINE BIOLOGY RESEARCH 7
9. microbial communities in each of the four sample types
differed both by location (Cape Cod and Boston
Harbor) and sample type (jellyfish or seawater) having
a significant effect (P = 0.001, RDA analysis followed
by a two-way ANOVA) (Figure 6). Communities at the
OTU level in A. aurita and N. bachei were significantly
different based on ANOVA and RDA analysis (P = 0.002).
Discussion
The results demonstrated that the two distantly related
jellyfish collected from the same geographic region
supported microbial communities that were different
from each other and the surrounding seawater at
both of the two sampling sites. Because the jellyfish
were encountered at different times of the spring/
summer season and were collected from two sites,
some of the differences in the jellyfish could be due
to site- or season-specific effects. However, major
dominant bacterial groups were observed in both jelly-
fish that suggest taxon-specific differences are present.
Gammaproteobacteria, specifically Vibrio spp. and
Photobacterium spp., dominated the microbial commu-
nity associated with Nemopsis bachei, but not that of
Aurelia aurita, suggesting host specificity. Vibrionales
form a component of the microbial community in par-
ticulate organic matter and biofilms (Dang & Lovell
2016), and commonly form associations with marine
organisms (Preheim et al. 2011). The high proportion
of Vibrionales sequences recovered on N. bachei and
their known low abundance as free-living in parallel
seawater strongly suggest that their growth is pro-
moted on the jellyfish, potentially by access to a suit-
able carbon source. Although this is not clear in the
case of N. bachei, some jellyfish have chitinous life
stages (Kawahara et al. 2013) which could support
Vibrionaceae and other chitinase containing bacteria
(Hunt et al. 2008). While Vibrionales are known to colo-
nize dead surfaces, some Vibrio spp. associate with the
gut and surfaces of copepods (Sochard et al. 1979; Hei-
delberg et al. 2002) and fish (Cerdà-Cuéllar & Blanch
2002), and V. fischeri forms a well-studied association
with squid (Guerrero-Ferreira et al. 2013). In this
study, some Vibrio sequences from N. bachei clustered
closely with V. harveyi recovered from squid light
organs (FJ227109, 99% identity) and coral environ-
ments (AB497061, 99% identity). Some Vibrio spp.
found in marine environments are also potential
human, fish or shellfish pathogens (Huq et al. 1983;
Wong et al. 1999; Bowden et al. 2002; Ottaviani et al.
2013). Due to the variety of possible functions of
Vibrio spp. in the marine environments, the association
in N. bachei could be commensal, mutualistic or para-
sitic. The genus Photobacterium (Vibrionaceae), which
accounted for 29% of the Gammaproteobacteria on
N. bachei, is also often present in symbiotic relation-
ships with marine organisms (Urbanczyk et al. 2011),
and thus could form such an association in N. bachei.
Some strains of Photobacterium have luminescent
properties (Kita-Tsukamoto et al. 2006) that could
benefit jellyfish feeding. Additional Pseudoalteromonas
spp. related sequences suggest N. bachei supports this
group of bacteria that is often found in marine
particles.
The majority of the Bacteroidetes sequences associ-
ated with N. bachei belonged to Flavobacteriaceae. Fla-
vobacteria are a dominant bacterial group in marine
environments, especially on marine snow, and
capable of degrading diverse complex organic material
such as cellulose and chitin, making them important
players in marine carbon cycling (Suzuki et al. 2001; Wil-
liams et al. 2013; Dang & Lovell 2016). Flavobacteria
dominated the microbial community in the guts of
the ctenophore Mnemiopsis leidyi A. Agassiz, 1865,
suggesting they are potentially assisting jellyfish in
prey digestion (Dinasquet et al. 2012). Of the Bacteroi-
dete phylotypes unique to N. bachei in this study, three
were of the genus Tenacibaculum and one sequence on
N. bachei had a close match with T. mesophilum (strain
NBRC 16308; AB681059, 99% identity), which was first
isolated from the marine sponge Halichondria okadai
(Kadota, 1922) (Suzuki et al. 2001). The closest
matches of the other two Bacteroidetes phylotypes
unique to N. bachei were T. soleae (AM989478, 95%
identity) from the wedge sole Dicologlossa cuneata
(Moreau, 1881), a known fish pathogen (Piñeiro-Vidal
et al. 2008, López et al. 2010, García-González et al.
2011) and Tenacibaculum sp. C28 originally recovered
from seawater (JX853817, 98% identity). A fish
Figure 6. Ordination plot based on phylum-level discrimination
in Redundancy Analysis. Each dot for Aurelia aurita and Nemop-
sis bachei in the graph represents one jellyfish individual. Both
constrained axes shown are significant (P = 0.001). Total var-
iance between groups explained by RDA was 37.5%, with
RDA1, RDA2 and RDA3 explaining 15.5%, 13.3% and 8.7% of
the variance, respectively (RDA3 not shown in the figure).
8 M. C. DALEY ET AL.
10. pathogen T. maritimum was previously reported in the
hydromedusa Phialella quadrata (Forbes, 1848) where
it may influence digestion of food particles (Ferguson
et al. 2010). Based on this and previous studies, jellyfish,
including N. bachei, may serve as vectors for several
Tenacibaculum spp. (Avendaño-Herrera et al. 2006, Fer-
guson et al. 2010, Delannoy et al. 2011).
Lactobacillales in Firmicutes was also specific to
N. bachei compared with the surrounding seawater.
Additionally, Rickettsiales within Alphaproteobacteria
were present in N. bachei but not in the Cape Cod sea-
water, Rickettsiales related to Neorickettsia accounting
for 20% of Alphaproteobacterial sequences on
N. bachei. Related but different sequences found in
A. aurita suggest importance of this group for jellyfish.
Rickettsiales include many endosymbionts or patho-
gens (Walker 1996) as well as the important marine
free-living SAR11 cluster of Alphaproteobacteria that
were distant to the sequences recovered from
N. bachei. The Neorickettsia sequences from N. bachei
were most closely similar to Ehrlichia sp. (AF206298,
91–92% similarity) and Neorickettsia helminthoeca
(U12457, 90–91% identity).
The results suggest that bacteria within Gamma-
and Alphaproteobacteria, Bacteroidetes, Firmicutes,
and possibly Cyanobacteria may associate with
N. bachei. These are typical seawater phyla whose
representatives also associate with other marine
animals such as corals (Harder et al. 2003), sponges
(Schmitt et al. 2012), copepods (Tang et al. 2010) and
ctenophores (Daniels & Breitbart 2012). Notably, a
common marine snow colonizer group Roseobacter
was not detected on the jellyfish. Although we can
only speculate on the function of the associations,
the distinct communities found in the cnidarians and
seawater suggest some of them are host-promoted
and taxon-specific.
Bacteria suggestive of both mutualistic and parasitic
capabilities were found also on A. aurita. Mycoplasma
within Tenericutes was specific to A. aurita compared
with all sample types, and represented a large pro-
portion of the sequences recovered from A. aurita,
suggesting the host promoted the association.
Results from this study and a previous study on cteno-
phores (Daniels & Breitbart 2012), suggest that Myco-
plasmatales are common associates in marine
jellyfish; however, Mycoplasmatales were not detected
in N. bachei, suggesting these associations are jellyfish
taxon-specific. Mycoplasmatales have been found in
the marine invertebrate bryozoan Watersipora cucullata
(Busk, 1854) (Zimmer & Woollacott 1983; Rottem 2003)
as well as in corals (Penn et al. 2006; Kellogg et al. 2009;
Neulinger et al. 2009). Some Mycoplasmatales
parasitize plants and animals to obtain nutrients, and
cause human illnesses such as pneumonia and infec-
tions (Rottem 2003; Pitcher & Nicholas 2005). One of
the strains clustering closely with sequences from
A. aurita was Mycoplasma mobile, first isolated from a
fish. Its genome analysis showed that M. mobile is
able to transport and metabolize several sugars (Jaffe
et al. 2004) which could aid in obtaining nutrients
from hosts such as jellyfish. Mycoplasma could be
obtaining nutrients from A. aurita, thus forming a com-
mensal, mutualistic or parasitic association. A likely
endosymbiont in the Mycoplasma genus was recently
reported for A. aurita in the Eastern North Atlantic
populations (Weiland-Bräuer et al. 2015). Our study
provides support to the idea that Mycoplasma spp.
are common endosymbionts in various subpopu-
lations/clades of A. aurita, although the mechanisms
of this association are unknown.
The Gammaproteobacteria Psychrobacter spp. (clus-
tering closely with P. immobilis; Figure 2), found to be
specific to A. aurita compared with the surrounding
seawater, contain species that have been isolated
from a wide range of habitats that vary in temperature,
salinity and oxygen levels (Bowman 2006). Thus, it is
difficult to speculate on the nature of the association
of A. aurita with this phylotype.
The high proportion of picocyanobacteria Synecho-
coccus spp. of the microbial community in A. aurita
was somewhat unexpected, since the jellyfish were
treated to empty their gut contents before preserving.
While some of the sequences could be remnants of the
gut contents, they could alternatively indicate more
stable epi- or endobiotic associations, or the cyanobac-
teria could have been entangled in the outer mucus of
the jellyfish. The mucus of A. aurita and other jellyfish
species is a rich source of labile carbon and can effec-
tively entrap nanoparticles (Patwa et al. 2015) which
could also lead to concentration of surrounding bac-
teria. While dominant free-living cyanobacteria in
coastal waters, Synechococcus spp. are also found in
mutualistic associations with marine animals such as
some sponges, where they provide organic carbon to
the sponges via photosynthesis, while the sponge
returns metabolic waste products useful to the bacter-
ium (Taylor et al. 2007). Clade GpIIa cyanobacteria have
been found in association with sponges (White et al.
2012) and the cyanobacteria Synechoccocus (strain
PCC7943) was found in association with corals
(Rohwer et al. 2002), suggesting that photosynthetic
nutrients and byproducts may play an important role
between the host and bacterium. Synechococcus sp.
strain CC9902 (clade IV), that grouped most closely
with sequences obtained from A. aurita (CP000097,
MARINE BIOLOGY RESEARCH 9
11. 99% identity), is a common component in coastal
surface waters of Southern California (Palenik et al.
2009), suggesting the sequences on A. aurita may
have been from either feeding or entanglement on
the jellyfish mucus (Patwa et al. 2015).
The clone libraries for different sample types are
composed of pooled libraries from several individuals
among which there was variability in sequences recov-
ered, hence the data suggest variability is present in
communities among jellyfish individuals. This may be
a real trend, but sequence coverage depth available
for this study is a limitation for drawing conclusions
about the community stability among the jellyfish indi-
viduals. However, the RDA analysis incorporates this
variability and even at this relatively small sample size
allowed separation of the communities in different
sample types. Deeper sequencing would allow a
more detailed assessment of these communities. All
primers have certain biases and it is possible such
biases influenced our data as well; however, the 16S
rRNA primers used in this study were designed as uni-
versal and have been used in comparative studies of
marine bacterioplankton communities (Morris et al.
2004; Treusch et al. 2009). Jellyfish blooms are patchy
and seasonal in the waters where sampling was con-
ducted. The two species typically occur at different
times of the year and were sampled in the spring
(A. aurita) and summer (N. bachei), which may have
influenced the results due to changing temperatures,
food availability, and other environmental factors. The
influence of seasonality on the microbiomes of these
jellyfish merits further study. The degree of anthropo-
genic influence at the sampling sites may also have
played a role in structuring the communities observed,
as Boston Harbor is influenced by pollution from a
major urban city, and the Cape Cod Bay experiences
at least some effects from elevated nutrients from
coastal activities.
The taxon-specific associations in the hydromedusa
N. bachei and scyphomedusa A. aurita demonstrated
by this and other studies overall suggest that the rela-
tive fitness of different jellyfish taxa plays a role in
shaping microbial communities in coastal ecosystems.
Low oxygen tolerant N. bachei may be promoted in
the zooplankton community in coastal and estuarine
waters under periodic hypoxia (Marshalonis & Pinckney
2007), a condition enhanced by eutrophication. The
reported microbial communities dominated by Vibrio
spp. are notable in the case of N. bachei that currently
appears to be expanding its range to European waters
(Frost et al. 2010). The observation of Mycoplasma spp.
in A. aurita in Western North Atlantic waters in this
study suggests this association is a stable symbiosis
found in several subpopulations of the species
(Weiland-Bräuer et al. 2015) in geographically distant
locations.
Acknowledgements
We thank Eugene Gallagher and Scott Morey (University of
Massachusetts Boston) for help with statistical analyses. Com-
ments from the anonymous reviewers and the Associate
Editor improved the manuscript.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
The work was supported by the University of Massachusetts
School of Marine Science to Pia Moisander and Juanita
Urban-Rich, and a National Science Foundation award
[grant number OCE-1130495] to Pia Moisander.
ORCID
Pia H. Moisander http://orcid.org/0000-0002-3262-3662
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Bacterial associations with the hydromedusa
Nemopsis bachei and scyphomedusa Aurelia
aurita from the North Atlantic Ocean
Meaghan C. Daley, Juanita Urban-Rich & Pia H. Moisander
To cite this article: Meaghan C. Daley, Juanita Urban-Rich & Pia H. Moisander (2016): Bacterial
associations with the hydromedusa Nemopsis bachei and scyphomedusa Aurelia aurita from
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