Bacterial community composition of the sedimentin the coastal regions of Kashima-Nada andKujukurihama, Japan
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言語: en
出版者: 国立研究開発法人

水産研究・教育機構

公開日: 2023-01-27
キーワード (Ja):
キーワード (En):作成者: 坂見, 知子, 宇田川, 徹
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所属: 水産研究・教育機構（退職）, 水産研究・教育機構
URL

https://doi.org/10.57348/00000113

水 研 機 構 研 報， 第 50 号，9 － 17， 令 和 ３ 年
Bull. Jap. Fish. Res. Edu. Agen. No. 50，9－17，2021

9

Bacterial community composition of the sediment in the coastal regionsof Kashima-Nada and Kujukurihama, Japan

Tomoko SAKAMI＊1 and Toru UDAGAWA＊2
Abstract: Environmental monitoring of marine coastal areas is becoming increasingly importantbecause of accelerated global climate change and rapid industrial development. The composition of
the bacterial community in bottom sediments is strongly related to the surrounding environment.
Thus, surface sediments were collected at the coastal regions of Kashima-Nada and Kujukurihama
to elucidate how bacterial communities vary where the confluence of the cold Oyashio and warm
Kuroshio Currents occur. The bacterial communities collected at water depths of 10 m weredifferent between the Kashima-Nada and Kujukurihama areas, but were not different at water
depths of 30 m. The chlorophyll a content in the sediment and bottom water temperature wereindicated as the major environmental parameters influencing the composition of the bacterial
communities. At 10 m depth in the Kujukurihama area, operational taxonomic units (OTUs) ofBacteroides, which are known as high molecular weight organic matter degraders, were abundant,
whereas OTUs of Nitrospinae and Nitrosospira, which are related to the nitrification process, wereless abundant. The taxonomic groups characteristic of the sediment seemed to be related to theproperties of organic matter quality in the sediment.
Key words: bacterial community composition, sediment quality, Kashima-Nada, Kujukurihama

Introduction

monitoring physical and chemical parameters is
not enough to evaluate integrated environmental

Terrestrial materials such as soil, inorganic

conditions for living organisms. As a biologicalnutrients, and organic matter are discharged into

parameter, macrobenthos fauna are often examined

the sea through river water flow or by land erosion,in order to monitor coastal environmental conditions.

with considerable consequences for the coastal

This requires time and labor, and the amount ofenvironment (Bergamaschi et al., 2012). In addition

data is less than what is obtained by physical andto industrial development on land, global climate

chemical monitoring. In contrast, approximatelychange, which is predicted to bring about increases

one hundred million bacterial cells can be observedin torrential rain and storms (Yagi et al., 2015), willin a single gram of marine sediment (Schmidt etchange material inputs from land to coastal areasal., 1998). Data collection for bacterial community(Philippart et al., 2011; Viitasalo et al., 2015). To deal

composition analysis is a mechanical processwith prospective environmental changes, we need tothat augments physical and chemical parametermonitor certain environmental parameters precisely.

measurement. Typically, millions of bacterial

Using physical and chemical monitoring techniques,sequences can be retrieved from one sample, and

it is now possible to obtain highly accurate data

they can be clustered into hundreds or thousands

owing to advances in measuring equipment andof species. Therefore, it may be possible to detect

information technology (Bean et al., 2017). However,certain integrated environmental changes which
2020年12月11日受理（Accepted on December 11, 2020）＊1
National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, 422-1 Nakatsuhamaura, Minami-ise, Mie, 5160193, Japan＊2
National Research Institute of Fisheries Engineering, Japan Fisheries Research and Education Agency, 7620-7 Hasaki, Kamisu, Ibaraki, 3140408, Japan
E-mail: sakami “at” affrc.go.jp

10

Tomoko SAKAMI and Toru UDAGAWA

cannot be detected by physical and chemical

and the exact dimensions of this band depend also

parameters alone.

on the year of the survey (Shimizu, 2001). Bacterial

Bacterial community composition of coastal bottom

communities in sediments may change in different

sediments is more diverse than that of seawater

ways from the larger organisms and may help

(Zinger et al., 2011). Community compositions are

elucidate bottom environmental conditions in more

often related to environmental conditions such asdetail.

the particle size of the sediment, and the dissolved

We examined bacterial community composition

oxygen concentration in the bottom water (Zheng

in the sediments collected at Kashima-Nada andet al., 2014), or the organic matter content in the

Kujukurihama by using 16S ribosomal RNA (rRNA)

sediment (Qiao et al., 2018). Salinity change in thegene sequences. By analyzing relationships between

brackish water area (Vidal-Durà et al., 2018) andthe community composition and sediment quality

anthropogenic contamination, such as metal andparameters, such as organic matter content andpolycyclic aromatic hydrocarbon contaminants

mud content, we aimed to clarify how the bacterial

from land (Sun et al., 2013), can also affect sedimentcommunity varies in this area, and how the sedimentbacterial communities. In land soil, bacterial

qualities influence or reflect these variations.

communities are more affected by the biochemical
Materials and Methods

conditions of the soil, such as organic matter content,
than by the origin or geographic location of thesoil (Lin et al., 2019). In marine bottom sediments,

Sample collection

however, it is not clear what difference the sea area

Sediment samples were collected at three sites

makes. Factors such as the geographical distanceadjacent to the shorelines at a water depth of 10 mfrom land, or overlying seawater characteristics

and 30 m, at the Kashima-Nada and Kujukurihama(the current type), may affect bacterial communities

beaches in July, August, and September 2017 (Fig.

together with the bottom environmental parameters1). The annual water temperatures ranged from 25℃

such as particle size or organic matter content.

(highest; range: 23-27℃) to 12.5℃ (lowest; range:

Kashima-Nada and Kujukurihama are open, large,

9-14℃) at Kashima-Nada, and from 26℃ (highest;

sandy beaches, which are located at the northernrange: 25-27℃) to 15℃ (lowest; range: 12-16℃) at

and southern parts of Cape Inubo, respectively, on

Kujukurihama area between 2014 and 2018 (Tokyo

the Pacific coast of Japan. In these areas, primaryDistrict Meteorological Observatory). A Smith-production is high, and there are high fisherycatches of bivalves and whitebait (Okunishi et al.,2000). The cold Oyashio Current and the warm
Kuroshio Current run along the Pacific coast of

140°E

141°E

142°E

Japan, and they meet at a confluence point, off
Pacific
Ocean

Cape Inubo. It is well known that the biologicalcommunity of the Pacific coast of Japan changes,
with Cape Inubo marking the border of the northernand southern fauna and flora (Shimizu, 2001). In

36°N

addition, the Tone river mouth, which is the largest

Cape Inubo

river in Japan, is north of Cape Inubo. Together

Kujukurihama

with the large amount of river water discharge andthe high wind in this area, a strong tidal stream

Kashima-Nada

35°N

occurs around Cape Inubo, and complex waterexchange and sediment transportation occurs (Yagiet al., 2002; Arai et al., 2006; Uzaki et al., 2016). The
distribution patterns of macrobenthos fauna vary
within a certain band north and south of Cape Inubo,

Fig. 1. Sample collection points at the coastal regionsof Kashima-Nada and Kujukurihama on the PacificFig. 1.Japan.
SampleOpencollection
pointsat the coastal
regionsandofcoast,
symbols
indicate
10 m depth,
Kashima-Nada
andKujyukurihama
onthePacific
coast,
solid symbols indicate 30 m depth.
Japan. Open symbols indicate 10 m depth, and solid
symbols indicate 30 m depth.

Bacterial community composition in coastal sediments

11

McIntyre grab sediment sampler (1/20 m2, RIGO,

taxonomic annotation using the Mothur Miseq

Osaka, Japan) was used to collect sediment samples.

standard operating procedure (SOP) (Kozich et al.,A surface sediment sample (top 2 cm) was collected2013). Inverse Simpson diversity index was alsousing a plastic corer of 23 mm diameter, and theestimated using this procedure.

sample was frozen immediately in a sterilized plastic

The analyses below were done using the statisticalbag. The sediment samples were kept at -60℃

package R version 3.5.3 (R Core Team, 2018).

until further processing. Temperature and salinity

Detrended correspondence analysis was performed

were measured using a multi-parameter handy

and produced an axis length of less than four,

conductivity temperature depth profiler (RINKO

indicating a linear relationship between community

Profiler, ASTD152, JFE Advantech, Nishinomiya,composition and the examined environmental

Japan).

parameters: temperature, salinity, median particle
diameter, mud content, ignition loss, and chlorophyll

Sediment quality analysis

a content. Therefore, relationships of the bacterial

The following variables were analyzed: (i) particle

community composition across the sampling sites

size was determined using a laser diffraction particle

were examined using non-metric multi-dimensional

size analyzer (SALD-3100; Shimadzu, Kyoto, Japan),scaling (NMDS) analysis, and relationships of the(ii) ignition loss was evaluated by igniting thebacterial community composition and environmental

sediment samples at 550℃ for 12 h, (iii) chlorophyllparameters were examined using redundancy

a content was determined by fluorescence using aanalysis (RDA). Relative abundance of subphyla

spectrophotometer (10AU, Turner Designs, San Jose,of the top three phyla, namely Proteobacteria,

USA).

Bacteroidetes, and Firmicutes, and phyla whose
relative abundance was more than 0.001 wereDNA extraction and sequencing

compared among four sampling areas: Kashima-

DNA was extracted from a 0.4 to 0.6 g sedimentNada-10 m, Kashima-Nada-30 m, Kujukurihama-10

sample using the Fast DNA SPIN Kit for soil (MPm and Kujukurihama-30 m. A heatmap figure was

Biomedicals LLC., Ohio, USA) according to themade using the 16 taxonomic groups that were

manufacturer’s instructions. Barcodes were attachedsignificantly different among the four areas (ANOVA,

to DNA fragments in a 2-step PCR amplificationp < 0.05).

that targeted the variable V1/V2 region of the 16S
rRNA gene based on the protocol of Sakami et al.

Results(2016). First PCR was conducted using 27Fm and338R primers (Kim et al., 2013), then the sequences

Environmental parameters

were modified by adding 34 and 36 bp snippets,

Median particle diameter (d50) was larger in therespectively, in order to later add molecular

Kashima-Nada-30 m, and mud content was higher

identifier (MID) tags. Pooled amplicons were paired-in Kujukurihama-30 m. Ignition loss was higher

end sequenced (2×300 bp) on the Miseq device

at Kujukurihama at a depth of 10 m and lower at(Illumina, Tokyo, Japan).

Kashima-Nada at a depth of 30 m. Chlorophyll acontent was higher at a depth of 30 m in both areas.

Bacterial community analysis
The sequences obtained by extraction wereBacterial community composition

quality filtered, and chimeras were removed using

The number of sequences obtained from sediment

the UCHIME algorithm (Edger et al., 2011) withprofiles ranged from 60,000 to 138,000 per sample.

alignment to the SILVA database (SSU_Ref_NR

The community coverage was estimated to bever. 119) reference alignment. Sequences that

more than 0.999 for all samples. The sequences

passed through the filtering process were divided

were clustered into 803 operational taxonomic units

into operational taxonomic units (OTUs) using a(OTUs). Community diversity (Inverse Simpson

3% similarity threshold and were identified withindex) ranged from 5.8 to 11.4, and it tended to be12

Table 1. Average values of environmental parameters andbacterial community
diversity at the sampling areas
Tomoko SAKAMI and Toru UDAGAWA

Table 1. Average values of environmental parameters and bacterial community diversity at the sampling areas

Kashima-Nada-10m
Kashima-Nada-30m
Kujukurihama-10m
Kujukurihama-30m

Central particle
diameter(um)

MudContent(%)

Ignition
Loss(%)

Chlorophyl acontent(ug/cm2)

Invsimpson
index

33.7b

187 b

0.18 b

1.4 bc56.3 b

6.8b

17.0b

33.8 b239 a0.05 b

1.4 c

203 a

7.4ab

21.6a

34.0 ab166 b0.36 b2.1 a88.8 b8.4ab

19.3ab34.3 a160 b0.99 a

1.8 ab

167 a

8.9a

Temp

Salinity

(°C)

(psu)

20.7ab* Numbers with different superscripts are different at the significance level of p < 0.05.
100%
90%

* Numbers with different superscripts are different Acidobacteria
at theActinobacteria
significance level of p < 0.05..
Bacteroidetes

80%
70%
60%
50%
40%
30%
20%

Kashima
10m

Kujukuri30m

JK1030SK1030
JK0830
AK0830SK0830SK0330

Kujukuri
10m

JS0930SS0930JS0630AS0630SS0630JS0330SS0330
JInu30SInu30JK1010SK1010
JK0810AK0810SK0810
JK0310AK0310SK03100%JS0910AS0910SS0910SS0610JS0610AS0610SS0310JS0310

10%

系列21
系列20
系列19
Chloroflexi
系列18
Cyanobacteria/Chloroplast
系列17
Firmicutes
系列16
Fusobacteria
系列15
Ignavibacteriae
系列14Latescibacteria
系列13
Nitrospinae
系列12Planctomycetes
系列11
Alphaproteobacteria
系列10
Betaproteobacteria
系列9Deltaproteobacteria
系列8
Epsilonproteobacteria
系列7Gammaproteobacteria
系列6Proteobacteria_unclassified
系列5
Spirochaetes
系列4Verrucomicrobia
系列3
etc
系列2
Bacteria_unclassified
系列1

Kashima
30m

Fig. 2. Bacterial community composition in the surface sediment collected at 10 and 30 m depths off the coastal
regions of Kashima-Nada and Kujukurihama in July, August and September, 2017.
0.3 the surface sedimenthigh at Kujukurihama(Table 1). Of
the OTUs, composition
33%
Fig. 2. Bacterial
communityin

to 53% belonged
to the phylum,collected
at 10 orProteobacteria,
30 m depths andoff the coastal
regions of Kashima0.2

the major subphyla
wereGammaproteobacteria
Nada andKujyukurihama
in July, August, and September of 2017.
(21%–30%) and Deltaproteobacteria (5%–21%).
Actinobacteria (3%–9%) and Acidobacteria (2%–6%)(Fig. 2).
The community composition of each sample wasplotted in two dimensions following NMDS (nonmetric multi-dimensional scaling) analysis (Fig. 3).
Bacterial communities at a depth of 30 m at both
Kashima-Nada and Kujukurihama were plotted
together in the top area of the graph. Bacterial
communities at a depth of 10 m at Kashima-Nada
were plotted below the 30 m communities, and those
off Kujukurihama were plotted in the bottom area of
the graph.

NMDS 2Other major phyla were Bacteroidetes (7%–33%),

0.1
0

-0.1
-0.2
-0.3

-0.7

-0.6

-0.5

-0.4

-0.3

-0.2

-0.1

0

0.1

0.2

0.3

NMDS 1Non-metric multi-dimensional
scaling plotof sedimentNon-metricmulti-dimensional
scaling
plot ofFig.Fig.
3. 3.
bacterial bacterial
communitiescommunities
with environmental
parameters.
Black
sediment
withenvironmental
symbols indicate the Kujyukurihama area, and gray symbols
parameters.
Black symbols
indicate
Kujukurihama
indicate the Kashima-Nadaarea. Opensymbols
indicate a depth of
10 andm andgraysolid symbols
indicate
30 m depth.
area,
symbols
indicate
Kashima-Nada area.
Open symbols indicate a depth of 10 m and solid
symbols indicate 30 m depth.

Bacterial community composition in coastal sediments

13

The relationships between the composition

the 10 m depth at Kashima-Nada, and the 10 mof the bacterial community and environmental

depth at Kujukurihama from the right. The Y-axis

parameters were examined using redundancy

represented 4% of the community variation. Bacterial

analysis (RDA) (Fig. 4). The X-axis represented 54%

communities at a depth of 10 m at Kujukurihamaof the community variation. Bacterial communities

were placed on this axis. Large directional arrows of

were placed in order of the areas of 30 m depth,

chlorophyll a content and water temperature were

RDA2-Percent variations explained 4.0％

along the X-axis, implying that these parameters
were strongly related to variation in bacterial

150

community composition. Small directional arrows

100

for mud content, salinity, and ignition loss were on

50

Temp

d50

the lower right. No obvious directional arrows were

Chla

Mud

0

observed along the Y-axis.

Sal

-50

The relative abundance of the major taxonomicILgroups, whose abundance was different among the

-100
-150

four sea areas, was shown in a heat map (Fig. 5).

-200

The taxonomic groups were clustered into two-250groups (cluster I and II), with the first cluster
-120

-100

-80

-60

-40

-20

0

20

40

60

80

100

RDA1-Percent variations explained 54％

divided further into three subgroups (cluster

Ia, Ib, Ic). Cluster Ia included Acidobacteria andFig.
4.
Redundancy
analysis(RDA)ofsediment
Proteobacteria, except for beta and epsilon types,
Fig. 4. Redundancy analysis (RDA) of sediment bacterial communities withenvironmental
symbolsb a c tparameters.
e r i a l c oBlackmmu
n i t i eindicates w i t theh Kujyukurihama
e n v i r o n m earea,n t aandl gray and abundance tended to be low at a depth ofsymbols indicate the Kashima-Nada area. Open symbols indicate 10 m depth, and solidparameters. Black symbols indicate Kujukurihama
symbols indicate 30 m depth. IL, Chl a, d50, and mud represent ignition loss,
10 m off the Kujukurihama coast. Cluster Ib
area,and mediangray particle
symbols
indicate
Kashima-Nada
chlorophyll
a content,
size, andmud content,
respectively.
included Chloroflexi and Ignavibacteriae, and thearea. Open symbols indicate 10 m depth, and solid
abundances tended to be low at a depth of 30 m
symbols indicate 30 m depth. IL, Chl a, d50, and mud
at Kashima-Nada and at Kujukurihama. Cluster
represent ignition loss, chlorophyll a content, median
Ic included Betaproteobacteria, Planctomycetes,

particle size, and mud content, respectively.

KashimaNada
10m

Kujukurihama
30m

KashimaNada
30m

JS0910AS0910SS0910SS0610JS0610AS0610SS0310JS0310JK1010SK1010
JK0810AK0810SK0810
JK0310AK0310SK0310JS0930SS0930JS0630AS0630SS0630JS0330SS0330
JInu30SInu30
JK1030SK1030
JK0830
AK0830SK0830SK0330

Kujukurihama
10m

Alphaproteobacteria
Proteobacteria unclassified
Gammaproteobacteria
Cluster Ia
Deltaproteobacteria
Acidobacteria
Chloroflexi
Cluster Ib
Ignavibacteriae
Betaproteobacteria
Planctomycetes
Clostridia
Cluster Ic
Spirochaetes
Nitrospinae
Sphingobacteriia
Verrucomicrobia
Cluster II
Flavobacteriia
other Bacteroidetes

Fig. 5. Hierarchically clustered heatmap of bacterial communities from the four areas at the phylum orsubphylum level. Rows represent the relative abundance of each bacterial group, and columns indicate different
sediment samples. The relative abundance of each bacterial taxon is depicted by color intensity with the legend
indicated at the top of the figure.

Fig. 5. Hierarchically clustered heatmap of bacterial communities
from the four areas at the phylum or subphylum level. Rows
represent the relative abundance of each bacterial group, andcolumns indicate different sediment samples. The relative
abundance of each bacterial taxon is depicted by color intensity

Tomoko SAKAMI and Toru UDAGAWA

Relative abundance

14

0.016

Nitrosospira OTU

bacterial community composition was different
between Kashima-Nada and Kujukurihama at depthsof 10 m, but no obvious difference was observed

0.012

at 30 m. The water depth, chlorophyll a content,
and mud content was related to the variation in

0.008

bacterial community composition in addition to thewater temperature, indicating that the bacterial

0.004

communities present in the examined areas0

environment rather than with the differences invaried primarily with the conditions of the bottom

KJ- KS- KJ- KS10m 10m 30m 30m

current. On land soil, bacterial community structureand diversity were shown to be affected moreby parent material differences or biogeographicalFig. 6. Relative abundance of a Nitrosospira OTU in
separation of the soil than the soil properties, such as
the four areas. KJ indicates Kujukurihama and KS
Fig. 6. Relative
abundance of a Nitrosospira OTU in theorganic
four matter content (Lin et al., 2019). In marine
indicates Kashima-Nada.
ecosystems, there is evidence that the benthic

areas. KJ indicates the Kujyukurihama and KS indicatesbacterial
the community composition is affected more
Kashima-Nada.
Clostridia, Spirochetes, and Nitrospinae, and theby the geographic location than the ecosystem typeabundance tended to be low at 10 m depths in theand time or upper water productivity (Zinger et al.,Kujukurihama area. Relative abundance of an OTU2011). Since the bacterial community compositions

affiliated to genus Nitrosospira accounted for 73% ofwere affected by sediment qualities rather thanbetaproteobacterial OTUs. It was low at a depth of

the geographical distance, we suggest that there

10 m at Kujukurihama (Fig. 6). Cluster II included

are considerable exchanges of sediment materials

Flavobacteriia, Sphingobacteriia, other Bacteroides,

between the northern and the southern areas ofand Verrucomicrobia, and the abundance tended toCape Inubo.

be high at 10 m depth in the Kujukurihama area.

It has been shown that bacterial community
composition in marine bottom sediments changes

Discussion

according to the primary production in the sea(Zinger et al., 2011). The Tone River water

It is well known that the fauna and flora change

discharge to the north side of Cape Inubo, increases

at the border of the northern and southern junction

primary productivity in both the Kashima-Nada andat Cape Inubo, on the Pacific coast of Japan. For

Kujukurihama areas, and the influence fluctuates

example, the distribution of marine bivalves andwidely with precipitation and wind conditions

snails changes from tropical to cold-water varieties(Arai et al., 2006). The primary productivity in theat the border of the Boso Peninsula (Shimizu, 2001).

Kashima-Nada area was estimated to be 0.4 g C/

The warm Kuroshio Current which runs along them /day, and 76% of the production was estimated towestern Japanese Pacific coast changes direction

depend on the regeneration of the nutrient due toto the east at Cape Inubo, leaving the main islandorganic matter degradation within the area (Okunishi

of Japan. Therefore, the Kujukurihama area is

et al., 2000). Although primary production and a

influenced by the warm Kuroshio Current. In

contribution from regeneration production were notcontrast, a confluence of the warm Kuroshio and theindicated at the Kujukurihama area, the taxonomic

cold Oyashio Currents occurs at the northern end offeatures observed in the bacterial community

Cape Inubo, the Kashima-Nada area. Moreover, thecomposition may indicate different biologicalfour examined areas, viz. the 10 m and 30 m depths

production processes between the two areas.

2

at the Kashima-Nada and Kujukurihama sites, had

Concerning the abundance of bacterial

different bottom environments as indicated by theirtaxonomic groups in the four sea areas, cluster IIparticle size and organic matter content data. The(which was abundant at 10 m at Kujukurihama)Bacterial community composition in coastal sediments

15

Acknowledgements

included Flavobacteriia, Sphingobacteriia andVerrucomicrobia, which belong to Bacteroidetes.
Bacteroidetes are generally considered to be

The authors greatly thank Dr. Hiroshi Yagi of thespecialists in the degradation of high molecular

National Defense Academy for fruitful discussions

weight organic matter (Thomas et al., 2011). The

about coastal environment management and thetotal organic matter (ignition loss) was high, anddevelopment of new monitoring techniques. The

the chlorophyll a content was low at the depth

authors also thank the crew of the R.V. Taka-Maruof 10 m at Kujukurihama, suggesting that thefor their support during sample collection. This work

sedimentary organic matter was relatively poor in

was supported by JSPS KAKENHI Grant Number

fresh material. Flavobacteriia are often observed

JP17H03317.

abundantly at the end of phytoplankton blooms
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Combining Historic and Contemporary Methods

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with Modeling and Socioeconomics to Fulfill

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useful for monitoring coastal environmental changes

Carbon Storage and Greenhouse-Gas Fluxes inbecause not only does it reflect the environmental

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