Elsevier

Journal of Marine Systems

Volume 196, August 2019, Pages 77-85
Journal of Marine Systems

Structure and diversity of the bacterial community of an Arctic estuarine system (Kandalaksha Bay) subject to intense tidal currents

https://doi.org/10.1016/j.jmarsys.2019.04.004Get rights and content

Highlights

  • First NGS survey of bacterial communities of Kandalaksha Bay Arctic estuarine system

  • Proteobacteria dominated in all samples with γ-Proteobacteria as its main fraction.

  • Diffused occurrence of Prochlorococcus (low or absent in polar waters) was recorded.

  • Community driving factors were water temperature and salinity (RDA analysis).

  • Water mixing by currents influenced distribution and composition of the communities.

Abstract

Kandalaksha Bay is a peculiar estuarine system located at the Arctic Circle within the White Sea semi-enclosed basin (Russia). This sub-extreme marine environment combines features of temperate and Arctic seas. Its unusual hydrodynamic is due to seasonal high runoff of freshwater (caused by inputs from rivers and abundant precipitations), and tidal currents generating intense mixing mainly of surface waters. In order to get a survey of the bacterial community of this zone, seawater was sampled, at various distances from the shore and depths, in areas selected in relation to the tidal current pattern. Bacterial assemblages were characterised by 454-pyrosequencing to obtain detailed information on their diversity and structure. The phylum Proteobacteria was the most predominant in all samples (abundance ranged from 67% to 96%), being the class γ-Proteobacteria its main fraction. Cyanobacteria was the second most abundant phylum (11–15%) in surface samples collected offshore in the main tidal stream, while it was rather scarce in the coastal samples and very low at the maximum depth. Unexpectedly, no presence of Synechococcus was detected; in addition, the diffused occurrence of Prochlorococcus, generally very low or absent in polar waters, could be considered another effect of global change. Bacteroidetes showed abundance ≥5% in surface and shallow waters (15 m). At the genus level, biodiversity clearly decreased in the offshore samples, in particular at the highest depth, were high prevalence of Halomonas was recorded (>65%).

The Redundancy Analysis revealed that water temperature and salinity represented the environmental factors determining the bacterial community structure. Moreover, the nMDS analysis evidenced high similarity only among samples taken in surface layers and involved in the water mixing by tidal currents, being the deepest sample (−70 m) the most dissimilar.

Introduction

Microorganisms represent the last boundary for life in regions that could not be colonised by other life forms. Those from extreme and sub-extreme cold environments, such as the highest mountains, the Arctic and Antarctic regions, provide optimal subjects for studying peculiar adaptation mechanisms and response to global change (Selbmann et al., 2012; Reboleiro-Rivas et al., 2013; Andrade et al., 2014). Obtaining information regarding the various groups within the microbial community of a certain environment is important for understanding their relative influence in the biogeochemical cycles and has become a fundamental ecological question (Cottrell and Kirchman, 2000; Zeng et al., 2013). In this context, further acquisition of environmental awareness requires detailed investigation of the microbial communities' composition, structure and functionality. This allows understanding the various and composite dynamics to which microorganisms are subject and evidencing possible strategies established to counteract repeated and intense environmental stress (Reboleiro-Rivas et al., 2013; Pesciaroli et al., 2015a).

Kandalaksha Bay (KB) is one of the three southern bays of the White Sea (WS), which is a rather small semi-enclosed Arctic sea (NW of Russia) and communicates with the Arctic Ocean through the Barents Sea. The water exchanges between the Barents Sea and the WS are limited, but establish a transport system for particulate material, microorganisms and biogeochemical species (Howland et al., 1999; Berger and Naumov, 2000; Pantyulin, 2003). KB is a complex insular estuarine system having a special hydrological regime with rather large sea level differences during tides (shallow, asymmetrical and semi-diurnal), causing great cyclic variations in depths and horizontal displacements of the coastline, and intense mixing of waters within 30 m from the surface (Melnikov et al., 2003; Savvichev et al., 2003). In some areas (i.e. the “Velikaja Salma” strait), both stratified and mixed regions are present. Actually, the topographic features of this area lead to an increase in tide height (up to 2.5 m), but especially in the tidal currents speed that can reach 80–120 cm/s (Pantyulin, 2003).

The pattern of currents is extremely complex and main tidal streams are often split in secondary flows by the various island; moreover, in some areas, peculiar mixing situations are generated also (Tzetlin et al., 1997; Berger and Naumov, 2000; Savvichev et al., 2003). The unique hydrodynamics of the bay is also affected by seasonal intense runoffs of freshwater, due to various rivers, streams and strong precipitations (Howland et al., 1999; Dolotov et al., 2005), which contribute to enrich the sea water with nutrients and microorganisms from the surrounding soils, forests and peatlands. On the other hand, these inputs, carrying particulate and humic substances, cause intense water darkening with consequent strong reduction of the photic zone, which is confined in the first 10 m on average, and could reach 15–20 m in days with the highest solar radiation (Bobrov et al., 1995; Kravchishina et al., 2013).

KB is subject to wide fluctuations of environmental parameters (Savvichev et al., 2003). Annual temperature variability is very high; although global change begins to mitigate it, the winter season is long and quite severe (the sea surface is sheltered by ice for 5–6 months) and the meteorological conditions tend to be very unpredictable. Air temperature may fall to −40 °C, but occasionally rises to few degrees above 0 °C, due to warm Atlantic air streams; water temperature is about −1 °C / −2 °C. In the rather short summer, air temperature can rise up to 30 °C (15–20 °C, on average), while seawater temperature can reach 15 °C on surface layers, but is subject to a fast drop and remains steadily around 0 °C below a few dozen meters of depth (Berger and Gorbushin, 2001; Pantyulin, 2003; Shaporenko et al., 2005; Vershinin et al., 2006)

In this region, organisms must adapt to variable environmental conditions in which factors (such as temperature and salinity) change frequently (Savvichev et al., 2004; Kravchishina et al., 2008), and communities must be functionally organised to cope with the effects of sudden stressing conditions (Pesciaroli et al., 2015b).

Microbial communities in the White Sea and, particularly in the KB area, have been scarcely investigated and very little is known about their structure, organisation and functionality. In addition, the majority of the studies characterised only the cultivable fraction of the communities (Savvichev et al., 2003, Savvichev et al., 2004; Kravchishina et al., 2008; Pesciaroli et al., 2015a). The sole attempt to depict KB total bacterial community composition and organisation was the preliminary work of Pesciaroli and co-workers (Pesciaroli et al., 2015b), carried out by the PCR-TGGE fingerprinting technique. Although somehow useful for a basic screening, this low-throughput method could only allow for partial characterisation of the community diversity, resulting in incorrect information in relation to its structure. To the best of our knowledge, no study by new generation sequencing techniques has been carried out yet.

This work was aimed at achieving a first high-resolution information on the bacterial diversity in the Kandalaksha Bay peculiar environment: the community composition and structure of sea-water samples, collected at various depths (0–70 m) in different sites selected in relation to tidal currents, were analysed by the 454 pyrosequencing.

Section snippets

Sample collection

Seawater samples (S1–S6) were collected in September 2008, at various depths and distances from the shore, in the “Velikaja Salma” strait (between Veliky Island and Cape Kindo peninsula), on the south-western coast of KB (Fig. 1). Samples were processed at the nearby “Nikolai Pertsov” White Sea Biological Station (WSBS, Moscow State University, “Lomonosov”).

Sampling sites were selected according to known flows of tidal currents that represent a branch of the main KB current, which enters the

Composition and diversity of the bacterial communities

A total of 53,870 validated reads were obtained, with an averaged value of 8978 reads/sample. Alpha diversity was estimated by Observed OTUs, Chao1, Shannon, and Good's coverage indices (Table 2). The Estimated Sample Coverage (ESC) was satisfactory (≥98%) for all samples. The number of observed OTUs and the estimated OTU richness (Chao1), ranged from 296 to 610 and from 411.02 to 669.40, respectively; the Shannon diversity index ranged from 2.82 to 6.65. The intertidal pool sample (S1) showed

Discussion

The present study focused on producing a first high-resolution characterisation of the bacterial communities of some KB areas selected according to known flows of tidal currents. Although sampling did not involve the entire KB gulf and an extensive campaign, this work provides the first in-depth description of the bacterial communities in this region. Actually, the whole area has been overlooked from the microbiological point of view, and only a limited number of studies regarding the bacterial

Conclusions

Kandalaksha Bay is an extremely dynamic marine transition area, where bacterial communities must be well adapted to repeated variations of environmental conditions, and where environmental factors (such as nutrient availability, temperature and salinity) change frequently. Although it represents an interesting study area, it has been overlooked from the microbiological point of view. This work was the first attempt to outline the KB bacterial communities with a high-throughput method (454

Acknowledgments

The authors wish to thank Prof. A. Tzetlin and Dr. A. Zhadan, Department of Biology, Moscow State University “Lomonosov”, for the kind support during the sampling campaign carried out at the “Nicolai Pertsov White Sea Biological Station”, Kandalaksha Bay, Russia. The research was partially financed by the Italian-Russian Institute of Ecological Formation and Research (IIRFRE, Istituto Italo-Russo di Formazione e Ricerche Ecologiche). The authors wish to thank Prof. D. Ercolini, University of

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