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Bacterial communities versus anthropogenic disturbances in the Antarctic coastal marine environment

  • Angelina Lo GiudiceEmail author
  • Gabriella Caruso
  • Carmen Rizzo
  • Maria Papale
  • Maurizio Azzaro
Review

Abstract

The Antarctic coastal marine environment is experiencing multiple stressors deriving from the concomitant effects of global environmental forcings and local disturbances from anthropogenic activities at research stations. Main contaminants include hydrocarbons, polychlorinated biphenyls, antibiotics and heavy metals, in addition to (micro)plastics which represent an emerging problem also in polar remote areas. Much more efforts are necessary to better clarify the effects of individual or co-occurring contaminants on the unique and fragile Antarctic environment, and to find novel and suitable solutions to avoid and mitigate contamination events. In Antarctica, autochthonous cold-adapted bacterial communities play a dual role as they sustain (and contribute to) the functioning of the Antarctic marine ecosystem, by supporting life under extreme conditions, and actively participate to the restoration of contaminated areas, thanks to their peculiar metabolic capabilities. Thus, they could represent a keystone for the environmental sustainability and restoration of contaminated Antarctic marine areas. Here, the interactions between the bacterial communities in coastal Antarctic marine environments and the human disturbance mainly derived from the proximity to research stations are reviewed.

Keywords

Antarctica Human pressure Anthropogenic activities Bacterial communities Contaminants Biodegradation 

Introduction

Human presence in Antarctica, mainly deriving from scientific activities at research bases, in addition to the presence of tourists/journalists during the summer (for short periods) and people in charge of maintaining the bases (annual), has increased in recent decades. The significant human impact linked to the ongoing research activities has been recognized and the scientific community has adopted specific measures to reduce possible negative effects, through the delivery of a Protocol to the Antarctic Treaty on Environmental Protection (Champ et al. 1992). Despite this Treaty, the risks for local contamination of coastal marine environment are increasing more and more, raising concerns about preserving the environmental quality of the continent (Kennicutt et al. 2010). The majority of stations are in coastal areas characterized by the absence of ice (Fig. 1). Land-based activities (such as waste disposal sites, sewage and wastewater disposal, fuel and oil spills) are the most frequent causes of environmental impacts (Stark et al. 2014). Indeed, human excreta (e.g. faeces, urine, sweat, and skin peeling), in addition to organic matter inputs, are indirect sources of synthetic chemical products (pharmaceuticals, recreational drugs, personal care products) and their metabolites (González-Alonso et al. 2017). Sewage and grey water originating from bathrooms, kitchens, and laundry facilities at Antarctic stations (as well as from fishing, tourism, research, and resupply vessels) also contain microorganisms that are alien to the Antarctic environment (e.g. human-derived faecal microorganisms) (e.g. Bruni et al. 1997; Delille and Gleizon 2003; Hughes and Thompson 2004; Martins et al. 2014), organic compounds (food waste and toilet paper) and chemicals (such as antibiotics, detergents, hydrocarbons, heavy metals, microplastics) with a different impact on the marine environments where they are discharged (Aronson et al. 2011). These activities at coastal stations can negatively affect the community composition, with consequent biodiversity loss, in the beneath marine coastal communities. Kennicutt et al. (2010) documented human impacts at McMurdo Station, one of the major concentration of anthropic activity in Antarctica, suggesting that the spatial extent of disturbance at Antarctic scientific stations can be restricted to within a few hundred meters from the base.
Fig. 1

Location of main coastal research bases in Antarctica

It is noteworthy that a number of pollutants can origin from outside Antarctica and transported over great distances by atmospheric and oceanic currents. Both the transport and deposition of persistent pollutants in Antarctica could be enhanced by climate change and global warming (Bargagli 2008; Stark et al. 2014). The cryosphere (which includes the frozen geosphere, i.e. permafrost, but also ice caps, snow, glaciers, sea-ice, lake ice, river ice, ice sheets, ice shelves) represents a reservoir/sink for organic and inorganic contaminants (particularly persistent organic pollutants and heavy metals) on time scales, from days to millennia (Poland et al. 2003; Grannas et al. 2013; Casal et al. 2018). In the coastal marine environment, sea-ice can entrap contaminants from seawater during the ice forming process and haul contaminants from sediments. Following perturbations from the climate change-driven warming or simply seasonal melting, contaminants can be released back into marine systems, entering the food webs. Bioaccumulation in organism tissues and biomagnification through the trophic levels (plankton to top predators) then occur (Lo Giudice et al. 2010a). Sea-ice (as well as the global cryosphere) thus becomes a key component of the contaminant cycles (Grannas et al. 2013) as chemical species that are stored therein are released following melting with significant environmental implications (Potapowicz et al. 2019).

Also because of the slow rates of the in situ degradation process, some contaminants (e.g. polyaromatic hydrocarbons, polychlorinated biphenyls, microplastics) remain detectable many years after their release, thus persisting in the environment and possibly accumulating along the food web, while petroleum hydrocarbons are more easily degraded in situ. Moreover, some contaminant agents can leach into the environment from forsake waste dumps and fuel-contaminated grounds, mainly in summer months when ice melting mobilizes entrapped pollutants. Thus, the anthropogenic perturbation of the marine environment may remain for long periods of time, even decades. Comprehending the ecological consequences of local impact from research bases, synergistically acting with global environmental forces, becomes fundamental in the administration and avoidance of environmental impacts in Antarctica (Stark et al. 2014; Flocco et al. 2019; Lo Giudice and Azzaro 2019). The human-induced stress experienced by this environment over the last half-century remains to be elucidated (Hughes et al. 2015). Marine microbes are highly sensitive to human perturbations, and environmental perturbations in general (Lo Giudice and Azzaro 2019). Fortunately, the sufficiently low impact experienced by Antarctica permit the individuation of main (micro)biota responses to the presence of contaminants. Since the Antarctic Treaty has prohibited the introduction of allochthonous species, a better knowledge of the natural capacity of the cold-adapted autochthonous microbiota to support remediation has become very useful for the risk assessment and for the improvement of in situ bioremediation processes and approaches (Vázquez et al. 2017; Flocco et al. 2019). A schematic view of the interactions between the main anthropogenic disturbances and the role played by bacteria in sustaining Antarctic coastal sites is given in Fig. 2.
Fig. 2

Ecological contributions of the bacterial community to the sustainability of the marine Antarctic environment. Global environmental changes and local anthropogenic activities at research stations are the main inputs of contaminants

In the following sections, chemical and sewage contamination from research bases and vessels, as well as atmospheric-driven pollution, and the microbial response to contamination are discussed. Focus will be on most common contaminants (Tables 1, 2) disturbing Antarctic microbial life and, in turn, influencing high organism health. The crucial role played by the cold-adapted bacterial communities in the functioning and sustainability of marine coastal Antarctic sites will be highlighted.
Table 1

Main pollutants occurring in biotic and abiotic matrices collected in the proximity of some Antarctic Research Stations

Pollutant(s)

Main source(s)

Research station(s)

Antarctic area

References

Hydrocarbons

Ship-to-shore fuel transfer; fuel storage; sewage release and waste disposal; research vessel supply; fossil fuel combustion; organic residue combustion; vehicle spills

Mc Murdo

West Antarctica

Klein et al. (2012)

Artigas

South Shetland Islands

Rodríguez et al. (2018)

Carlini

 

Curtosi et al. (2007)

Dauner et al. (2015)

Comandante Ferraz

South Shetland Islands

Martins et al. (2004)

Bícego et al. (2009)

Scott Base

West Antarctica

Aislabie et al. (1999)

Antibiotics

Pharmaceuticals; personal care products

Gondwana

West Antarctica

Wang et al. (2016)

Jang Bogo

 

Eduardo Frei Montalva

South Shetland Islands

Hernández et al. (2019)

Bellinghausen

 

McMurdo

West Antarctica

Emnet et al. (2015)

Scott

  

Heavy metals

Improper disposal practices; waste incineration; vehicle spills; outflow of poorly treated sewage

Comandante Ferraz

South Shetland Islands

Santos et al. (2005)

McMurdo

West Antarctica

Kennicutt et al. (1995)

Lenihan (1992)

Scott

West Antarctica

Sheppard et al. (2000)

Emnet et al. (2015)

Polychlorinated biphenyls

Improper waste disposal

Mario Zucchelli

West Antarctica

Focardi et al. (1995)

Zhongshan

West Antarctica

Mwangi et al. (2016)

Mc Murdo

West Antarctica

Crockett and White (2003)

Comandante Ferraz

Machu Picchu

Henryk Arctowski

South Shetland Islands

Combi et al. (2017)

Microplastics

Personal care products; release of plastic debris; fibres from synthetic textiles; microbeads in cosmetics

Mario Zucchelli

West Antarctica

Munari et al. (2017)

Cincinelli et al. (2017)

Rothera

Antarctic Peninsula

Reed et al. (2018)

Machu Picchu

South Shetland Islands

Waller et al. (2017)

They generally show potential toxicity to organisms and the capacity for bioaccumulation and biomagnification

Table 2

Examples of accidents, causing oil spills or vessel sinking, occurred in Antarctic and sub-Antarctic marine areas in the last 30 years

Antarctic sites

 

Vessel or research bases

Year

Hydrocarbons released (approx. liters, hydrocarbons)

Anvers Island

Palmer Archipelago

MS Bahia Paraiso

1989

600,000, diesel and jet fuel

King George Island

South Shetland Islands

BIC Humboldt

1989

No details

Crozet Islands

 

Alfred Faure Base

1997

20,000, diesel fuel

Deception Island

South Shetland Islands

MS Nordkapp

2007

700, diesel fuel

Bransfield Straits

South Shetland Islands

MS Explorer

2007

185,000, diesel fuel

Wilhelmina Bay

Antarctic Peninsula

MS Ciudad de Ushuaia

2008

No details

Ross Sea

 

In Sung no. 1 (Fishing vessel)

2010

No details

Ross Sea

 

Jung Woo 2 (Fishing vessel)

2012

No details

Cold-adapted bacteria: a brief description

The term “cold-adapted bacteria” collectively indicates bacteria indigenous to cold environments and includes both psychrophilic (cold-loving) and psychrotrophic (cold-tolerant or psychrotolerant) species (Morita 1975). Cold-adapted bacteria overcome the effects of low temperature (often in combination with additional environmental constraints) by a number of modifications at both structural and physiological levels (Pearce 2012). Most modifications do not merely derive by a short-term acclimatization, but persist and may be genetically regulated (Chintalapati et al. 2004). Cold-adapted bacteria are able to modulate the protein content of the cell membrane, the chain length of fatty acids, the proportion of cis to trans fatty acids and the type of carotenoids synthesized to withstand cold shock (Lo Giudice and Rizzo 2018; Tribelli and López 2018). Changes in other bacterial envelope components have been less investigated. For example, lipopolysaccharides are essential for the active growth of cold-adapted bacteria at low temperature. They modulate the flexibility and turgor pressure of the cell envelope, cell permeability and surface area to volume ratio (S/V) (Benforte et al. 2018). In Gram-positive bacteria both the cell wall and the inner membrane play a key role in the cold adaptation as they preserve the cell against ice-caused disruption and/or osmotic pressure alterations.

By a functional point of view, also considering the degradation of chemicals, cold-adapted bacteria are able to maintain enzyme-catalyzed reactions at an efficient rate for low temperature. Cold-adapted enzymes are up to ten times more active at low temperatures than that of their mesophilic counterparts (Feller and Gerday 2003) thanks to an uncondensed three-dimensional structure in the whole protein and the destabilization of the active site. These features make the catalytic centre more flexible (and often larger and more accessible to ligands at low energy costs) at temperatures that otherwise led to limit molecular motions by freezing (Lo Giudice and Rizzo 2018). The bacterial survival under extreme conditions is also possible thanks to the presence of other proteins (e.g., cold-shock proteins, cold-acclimation proteins, and heat shock proteins), which regulate a number of vital processes (such as transcription, translation, protein folding and membrane fluidity). The synthesis of cryoprotective compounds (e.g., glycine, betaine, sucrose and mannitol, as well as antifreeze and antinucleating proteins, exopolysaccharides and polyhydroxyalkanoates), which avoid the occurrence of ice crystals inside cells (causing structural damage and osmotic imbalance), acts at translation or transcriptional level stabilizing the mRNA, avoid the cold denaturation and autolysis of extracellular enzymes, lowers the freezing point and ice nucleation water temperature or influences the formation of biofilm and motility under cold conditions (Nichols et al. 2005; Ayub et al. 2009; Lo Giudice and Rizzo 2018).

All the above cited features are at the basis of the dual role played by cold-adapted bacteria in sustaining Antarctic ecosystems, as they give a crucial contribution to the functioning of ecosystem itself by supporting life under extreme conditions and are key organisms in the restoration of contaminated areas (Flocco et al. 2019).

Petroleum hydrocarbons

Hydrocarbons from petroleum are the main potential contamination agents in the Antarctic environment and mainly derive from fuel used for transport, ships, power generation, aircraft, and heating. Storing fuel at Antarctic research bases requires a ship-to-shore transfer that poses an additional, even if controlled, contamination risk (Brown et al. 2016; Vázquez et al. 2017). Moreover, accidental spills in Antarctica have became unfortunately more frequent due to the increasing vessel traffic deriving from tourism, fishing, research and supply vessels insisting in the area (for a review, see: Ruoppolo et al. 2013; Lo Giudice and Fani 2015; Brown et al. 2016) (Table 3). The risk of accidents and contamination are worsen by extreme weather, ice and isolation that likely limit a prompt action in case of pollution incident. Based on the type of fuel, variable proportions of aliphatic (more easily degradable) and polycyclic aromatic hydrocarbons (PAHs; more toxic and persistent than aliphatic hydrocarbons) can reach the environment. After their release into the marine environment, petroleum hydrocarbons undergo a gradual weathering process due to natural mechanisms (e.g. evaporation of the volatile fraction, surface spreading, oil-in-water dispersion, water-in-oil emulsification, dissolution, lixiviation and photooxidation). Microbial degradation also highly concurs to the natural attenuation of environmental oil contamination. All these chemical, physical and biological processes are influenced by low temperature, as in cold environments oil viscosity increases (thus reducing its spreading in aquatic matrices), short-chain alkanes (< C10) volatilize in longer times (with an increase in their toxicity towards microbes), and their water solubility increases, thus delaying the onset of biodegradation (Margesin and Schinner 1999). Moreover, the low temperature slows down the biodegradation process in cold habitats by affecting many biochemical reactions.
Table 3

Examples of studies on the response of bacteria to anthropogenic contaminants in Antarctic coastal areas

Matrix

Antarctic site

 

Microbial capacities

References

Hydrocarbon oxidation

PCB oxidation

Heavy metal tolerance

Antibiotic resistance

Seawater

Terra Nova Bay (Ross Sea)

West Antarctica

+

+

+

 

Yakimov et al. (1999, 2004)

De Domenico et al. (2004)

Michaud et al. (2004, 2007)

Pini et al. (2007)

Lo Giudice et al. (2010b)

Caruso et al. (2018b, in press)

 

Ushuaia

Sub-Antarctica

+

   

Prabagaran et al. (2007)

 

Anvers Island,

Antarctic Peninsula

   

+

Miller et al. (2009)

Sediment

Terra Nova Bay (Ross Sea)

West Antarctica

 

+

+

+

Lo Giudice et al. (2013)

 

Windmill Bay

 

+

   

Powell et al. (2003, 2005)

 

Winter Quarters Bay

  

+

  

Tumeo and Guinn (1997)

 

Whalers Bay

South Shetland Islands

  

+

+

Tomova et al. (2015)

Seaice/seawater

Terra Nova Bay (Ross Sea)

West Antarctica

+

   

Pepi et al. (2005)

Benthic organisms

Terra Nova Bay (Ross Sea)

West Antarctica

  

+

+

Mangano et al. (2014)

       

Caruso et al. (2018a)

 

Maxwell Bay

Antarctic peninsula

  

+

+

González-Aravena et al. (2016)

The response of autochthonous marine bacteria to a potential oil spill in the Antarctic marine environment can be only hypothesized basing on a few laboratory-scale experiments, as reports on this issue mainly dealt with terrestrial sites. However, some evidences suggest that cold-adapted marine bacterial consortia could probably attenuate hydrocarbon contamination by carrying the biodegradation process under in situ conditions (Vázquez et al. 2017). In fact, the controlled contamination of Antarctic marine matrices by hydrocarbons generally determines the stimulation of bacterial growth and the relative increment of hydrocarbon degrader increment by several orders of magnitude (e.g. Delille and Delille 2000; Powell et al. 2005). An oil spill could also cause shifts in the bacterial community composition. Yakimov et al. (2004) observed the appearance of novel taxonomic groups and an evident raising in the relative abundance of Gammaproteobacteria (about 90% of screened clones) in seawater samples collected at Terra Nova Bay (Ross Sea), beneath the Italian coastal Base “Mario Zucchelli”, and artificially contaminated with hydrocarbons. Colwellia and Oleispira members were enriched following hydrocarbon contamination, thus suggesting their potential involvement in the removal of hydrocarbons after a spill. In the same study, the bacterial community from the Adelie Cove, a pristine site within the ASPA no. 161, diversely reacted to the presence of hydrocarbons.

Contrarily to Yakimov et al. (2004), Prabagaran et al. (2007) reported on the predominance of Alphaproteobacteria in sub-Antarctic seawater, off Ushuaia, added with the water soluble fraction of crude oil. However, members of the genera Psychrobacter, Arcobacter, Formosa, Polaribacter, Ulvibacter and Tenacibaculum were found exclusively in crude oil contaminated seawater.

Powell et al. (2003) observed that the microbial community structure patterns in coastal Antarctic sediments, from impacted (hydrocarbons and heavy metals) and non-impacted locations, corresponded to anthropogenic environmental variables, more likely due to human activities in the region. The same authors reported on the short-term effect of diesel oil and two types of lubricants (biodegradable or synthetic) in a field observation on sediments of an Antarctic pristine site (Powell et al. 2005). The bacterial communities in sediments treated with diesel oil and synthetic lubricants significantly differed from the control.

Searching for catabolic genes is useful to establish the biodegradative potential, and the predominant catabolic pathways, of the microbial communities inhabiting a certain environment (Luz et al. 2004). Muangchinda et al. (2015) reported the presence of hydrocarbon catabolic genes in sediments next to the Syowa Station in Antarctica, suggesting that autochthonous bacteria have the potential ability to utilize hydrocarbons (mainly PAHs) and that bioremediation strategies could be applied also in Antarctic sediments.

A number of Antarctic marine bacteria from seawater (e.g., water column, sea-ice/seawater interface, surface seawater) are capable of utilizing hydrocarbons (both aliphatic and aromatic) as the sole carbon and energy source at low temperatures, suggesting that they very likely might play a pivotal role in the in situ biodegradation of hydrocarbons. They mainly belong to Actinobacteria (e.g. genera Rhodococcus and Arthrobacter) and Proteobacteria (e.g. genera Alcaligenes and Oleispira) (De Domenico et al. 2004; Michaud et al. 2004; Yakimov et al. 2004; Pini et al. 2007; Lo Giudice et al. 2010b; Kube et al. 2013). For example, Michaud et al. (2004) reported Rhodococcus and Arthrobacter isolates from Antarctic coastal areas showing different metabolic abilities for hydrocarbon degradation at different temperatures (as proven by gas-chromatographic analyses). Similarly, Pini et al. (2007) observed complex interactions and a functional complementation between Rhodococcus and Alcaligenes isolates when grown together in the presence of diesel fuel.

A number of hydrocarbon-oxidizing bacteria (manly Actinobacteria and Gammaproteobacteria) were isolated from surface seawater along the Victoria Land coast (Lo Giudice et al. 2010b). Phylotypes were differently distributed among the sites, even if Actinobacteria evidently predominated everywhere. Interestingly, different patterns of hydrocarbon utilization were shown by the isolates, with n-tetradecane and n-dodecane (among aliphatic hydrocarbons) that were more frequently (or exclusively) utilized than aromatics, strengthening the idea that bacterial consortia, consisting of bacteria with diversified substrate specificities, can efficiently utilize complex hydrocarbon mixtures (Lo Giudice et al. 2010b; Lo Giudice and Fani 2015).

Further insights into hydrocarbon-oxidizing bacteria from a coastal Antarctic site (Road Bay, Terra Nova Bay, at the sea–ice/seawater interface) were provided by Yakimov et al. (2004). Isolates from crude oil enrichments grew on different substrates, such as tetradecane, naphthalene and/or biphenyl. This study reported isolate Oleispira strain RB-8T (Yakimov et al. 2003), a marine obligate hydrocarbonoclastic bacterium, whose metabolism is restricted to the linear and branched aliphatic, saturated and non-saturated hydrocarbons and their derivatives (fatty acids or alcohols) (Kube et al. 2013). Genes for alkane monooxygenases/fatty acid desaturases and one P450 cytochrome, likely involved in terminal hydroxylation of hydrocarbons, were harboured by the Oleispira antarctica genome (Kube et al. 2013) and simultaneously expressed in O. antarctica cells grown on tetradecane. This makes O. antarctica a species ecologically competitive in cold environments and encourages its use in oil spill mitigation processes in polar areas (Kube et al. 2013).

The availability of hydrophobic pollutants, such as hydrocarbons, can be enhanced by employing several strategies including biosurfactant-mediated solubilization (Cameotra et al. 2010; Rizzo and Lo Giudice 2018). To date, such capability has been observed only for few Antarctic hydrocarbon-oxidizing bacteria from seawater (Yakimov et al. 1999; Pepi et al. 2005; Pini et al. 2007; Lo Giudice et al. 2010b) and sediment (Malavenda et al. 2015), most of which belong to the genus Rhodococcus. This latter has being recognized as an efficient hydrocarbon degrader, due to its capability to utilize a plethora of organic compounds, biosurfactant production, and ubiquity and persistence in the environment, even in cold areas (Lo Giudice and Fani 2015). Recently, an emulsifying activity on different hydrocarbons (e.g., tetradecane, hexane, octane, hexadecane) has been reported for extracellular polymeric substances (EPS) isolated from Antarctic bacteria, both free-living (genus Marinobacter; Caruso et al. 2019) and associated to Porifera (genera Colwellia, Winogradskyella, Shewanella; Caruso et al. 2018a). These findings remark the high biotechnological potential of cold-adapted bacteria as novel and underexplored sources of exploitable molecules to be applied in the preservation and sustainability of Antarctic cold-areas (Lo Giudice and Rizzo 2018).

Polychlorinated biphenyls (PCBs)

Polychlorinated biphenyls are among persistent organic pollutants. They reach the environment through several anthropic processes and show harmful effects at ecological and human health levels. Since 1960s, despite their remoteness, the presence of PCBs has been reported in biotic and abiotic matrices at both poles (Bhardwaj et al. 2018). Pathways suggested as source of PCB contamination in Antarctica include long-range transport by atmospheric and oceanic currents (Gambaro et al. 2005), local contamination due to improper disposal practices and/or waste burning and dumping at research stations (causing the pollution of Antarctic atmosphere), local accumulation due to biotic activities, and migratory organisms (mainly seabirds and whales) with their excrements and carcasses (Negoita et al. 2003; Montone et al. 2005; Choi et al. 2008; Lo Giudice et al. 2010a; Bhardwaj et al. 2018; Gao et al. 2018). In the marine environment PCBs cannot be easily dispersed and accumulate in sediments (representing the natural sink of pollutants) and enter the trophic webs. A number of organisms have get contaminated by PCBs, such as benthic organisms, zoo- and phytoplankton, fish, seabirds and marine mammals (e.g., Negri et al. 2006; Corsolini et al. 2011; Zhang et al. 2013). Bacteria are at the base of the transfer process of these toxic chemicals to higher trophic levels (Lo Giudice et al. 2013). Tumeo and Guinn (1997) observed the occurrence of PCB-degraders (approximately 104 microbes per gram of wet sediment on agar plates amended with PCBs) in marine sediments from the Winter Quarters Bay (McMurdo Sound). However, according to Kennicutt et al. (2010), PCB concentration in sediments at McMurdo Sound is similar to that in suspected source materials, so that limited capacities to degrade such chemicals are probably possessed by in situ microbes, allowing contaminants to persist tens to hundreds of years if natural processes are the only removal process.

Despite their detection in the Antarctic marine environment, certain PCB congeners, mainly among less chlorinated ones, can be degraded by few Antarctic cold-adapted bacteria from seawater (Yakimov et al. 1999; Michaud et al. 2007) and sediments (Lo Giudice et al. 2013) at Terra Nova Bay (Ross Sea), suggesting that bacterial communities could prefer less recalcitrant compounds for their growth. Recently, as a first attempt, we investigated on the PCB-degrading fraction of Antarctic sponge-associated bacterial community (unpublished data). As filter-feeders, Porifera actively filter large volumes of water, collecting suspended particles and microorganisms for their food requirements. Thus, particle-associated contaminants, including PCBs, may be also ingested and then accumulated in the animal tissues (Negri et al. 2006). Outer surfaces and interstices of ostia and oscula of Porifera are colonized by prokaryotes, which may be particularly prone to the utilization of contaminants accumulated in the tissues of sponge. Bacterial isolates from enrichment cultures of Mycale (Oxymycale) acerata grew in the presence of Aroclor 1242, a commercial PCB mixture, as the sole carbon source (unpublished data).

Overall, to date Antarctic PCB-utilizers are mainly among Actinobacteria (genera Rhodococcus and Arthrobacter) and Gammaproteobacteria (genera Pseudoalteromonas, Shewanella, and Psychrobacter). Interestingly, Psychrobacter, Pseudoalteromonas, Arthrobacter and Rhodococcus spp. from Antarctic sediments were strongly related (97–99% of similarity) to PCB-degraders from seawater collected from the same area (Yakimov et al. 1999; Michaud et al. 2007), thus indicating bacterial species common to both compartments. Finally, the higher percentage of PCB-oxidizing bacteria in sediments than seawater (Michaud et al. 2007) suggests that a pivotal role could be played by PCBs accumulated in sediments in selecting bacterial populations (Lo Giudice and Fani 2015).

Heavy metals and antibiotics

Heavy metals and antibiotics can naturally exist in the environment as they derive from a number of natural phenomena. However, their amounts in Antarctica is increasing more and more due to the anthropogenic activities. To understand the role played by the bacterial community as a reservoir of resistance genes in pristine environments, such as Antarctica, a number of experiments (see below) have been carried out on bacterial tolerance to heavy metals and antibiotics.

Heavy metals

The pathways through which heavy metals reach the Antarctic continent are similar to those already described for PCBs, i.e. long-range transport by mass flow in the atmosphere and water, improper disposal practices and/or incineration of waste produced at research bases, dumping of solid and liquid waste, shipping, vehicle spills, and outflow of poorly treated sewage from half a century of human activity (Negri et al. 2006; Lo Giudice and Fani 2015). As for other pollutants, current and abandoned research stations are often the origin of a local-scale heavy metal contamination. High levels of heavy metals have been detected in sediment, seawater and organisms all around Antarctica (e.g. Kahle and Zauke 2003; Dalla Riva et al. 2004; Runcie and Riddle 2004; Negri et al. 2006; Vodopivez et al. 2015; Trevizani et al. 2018).

Bacteria can absorb, accumulate (by either a passive metabolism-independent or an active metabolism-dependent process) and transform heavy metals in most food chains (De Souza et al. 2006). Heavy metal tolerance, often resulting in a multi-tolerance, has been detected in Antarctic bacteria isolated from seawater (De Souza et al. 2006; Caruso et al. 2018b, in press), sediment (Lo Giudice et al. 2013; Tomova et al. 2015) and benthic organisms (Mangano et al. 2014; González-Aravena et al. 2016; Caruso et al. 2018a). Such studies highlighted the high incidence of tolerance to metals, demonstrating that bacteria can cope and/or adapt to their occurrence even in environments characterized by a low human-impact (Lo Giudice and Fani 2015). Further, the tolerance to heavy metals is often strongly dependent on the level of metal concentrations in the considered sampling area (Tomova et al. 2015). For example, Lo Giudice et al. (2013) observed a high susceptibility level towards mercury in bacteria isolated from sediments at Terra Nova Bay, where mercury concentration is among the lowest ever reported for coastal marine environments (Bargagli et al. 1998): this suggested that the bacterial communities are probably not adapted to the presence of this heavy metal in their surrounding environment. Isolates from the Antarctic sponge Hemigellius pilosus (Kirkpatrick 1907) showed slightly more tolerance to mercury than bacteria from sediments (Mangano et al. 2014). Conversely, cadmium (whose content in sediments and organisms of the Terra Nova Bay is considerably high) was better tolerated (Negri et al. 2006; Lo Giudice et al. 2013; Mangano et al. 2014). A similar finding has been reported by González-Aravena et al. (2016) in bacteria isolated from the sea urchin Sterechinus neumayeri and tolerating zinc, a metal that was present at high concentrations in the echinoderm tissues. Tolerance patterns shown by sediment and sponge-associated isolates (Lo Giudice et al. 2013; Mangano et al. 2014) appear to be more likely strain- rather than species-specific, indicating a possible process of tolerance acquisition or loss. Bacterial resistance to heavy metals (and antibiotics) was probably associated with plasmids (Tomova et al. 2015; González-Aravena et al. 2016), thus raising the probability that autochthonous Antarctic bacteria can acquire multi-metal resistance traits also via horizontal gene transfer (for example through genes harboured by non-native microorganisms) (Lo Giudice and Rizzo 2018).

Among the adaptive strategies developed by microorganisms to counteract the heavy-metal stress, the secretion of extracellular polymeric substances (EPSs) can act as detoxifying agents as they segregate cations (due to their negative charges) and retain them into their matrix (Wei et al. 2011; Huang and Liu 2013). In this regard, recently Caruso et al. (2018b) observed that stimulation of EPS production allowed an Antarctic EPS-producing Pseudoalteromonas isolate from coastal seawater to tolerate mercury and cadmium at high concentrations. This capability was probably related to the presence of uronic acids and sulfate groups in the EPS molecules, which can bind cations. Monitoring EPS production in the presence of mercury and cadmium showed that the EPS amounts increased at increasing heavy metal concentrations, revealing a bacterial adaptation to the tested stress conditions (Caruso et al. 2018b). The produced exopolymers could be exploited in the bioremediation (as heavy metal chelators) of heavy metal-contaminated cold marine environments, highlighting again the high biotechnological potential of the Antarctic indigenous microbiota.

Antibiotics

At the time of writing of this review, the occurrence of antibiotics, as well as other pharmaceuticals, in the Antarctic marine environment has been seldom documented. Emnet et al. (2015) first investigated on pharmaceuticals and personal care products (such as soaps, lotions, toothpastes, sunscreens, fragrances, and moisturizers) as contaminant agents in the Antarctic coastal environment, including organisms. González-Alonso et al. (2017) reported on the presence of pharmaceuticals (e.g. analgesics, anti-inflammatory drugs and antibiotics) and recreational drugs (licit and illicit) in different freshwater bodies (streams, ponds, a glacier drain and wastewater discharge) in the Northern Antarctic Peninsula. In particular, antibiotics were among those compounds occurring at the highest concentration in the samples. Antibiotic residues and antibiotic resistance genes/bacteria directly derive from the presence of humans in Antarctica and reach the marine environment by sewage discharge (parts of the antibiotics given to humans are in fact excreted unaltered in faeces and urine), posing serious risks to the environment. Following their release, many antibiotics and their residues may remain in the aquatic environment for long time (often months) altering the microbiosphere by interfering with microbial activities and the biogeochemical cycling (Mangano et al. 2014). Antarctica, as a quite pristine environment, offers the best chance to assess pre-antibiotic era levels of resistance among native bacterial populations (Lo Giudice and Fani 2015). However, only few data are available on the antibiotic resistance in Antarctic marine bacteria, with few studies that have been carried out, generally in parallel with heavy metal tolerance, in bacteria isolated from seawater (De Souza et al. 2006; Miller et al. 2009; Lo Giudice et al. 2010b, 2012), sediments (Lo Giudice et al. 2013) and some organisms (Miller et al. 2009; Mangano et al. 2014; González-Aravena et al. 2016). Psychrotrophic bacteria are generally resistant to conventional antibiotics (e.g., ampicillin, chloramphenicol, kanamycin and streptomycin) (De Souza et al. 2006; Miller et al. 2009; Lo Giudice et al. 2013; Mangano et al. 2014; González-Aravena et al. 2016). Interestingly, Miller et al. (2009) observed that the frequency of antibiotic resistant bacteria increased with proximity to the Palmer Station (Western Antarctic Peninsula), with multiresistant bacteria also increasing, thus suggesting that human presence has interfered with the resistome of the native bacterioplankton community.

More recently, Hernández et al. (2019) determined the occurrence of pharmaceuticals, with special emphasis on antibiotics, in wastewater and seawater from King George Island (South Shetland Islands). This area hosts many scientific and logistic facilities, including several permanent stations, and is experiencing an increased tourism presence in summer. The parallel finding of bacterial resistance for some antibiotics (e.g., trimethoprim and the group of quinolones) is in accordance with the presence of such compounds in the samples, demonstrating that the anthropogenic impact derived from the pharmaceutical consumption in the area.

The increased occurrence of antibiotic resistance genes, which have been mobilized to the polar Antarctic regions following anthropogenic presence was also shown by Hernández and González-Acuña (2016). The high frequency of antibiotic resistance observed in Antarctic marine bacteria is surprising being a pristine environment where the exposure of biota to antibiotics and the anthropic pressure is limited. In this regard, in a study on maritime Antarctica, Tam et al. (2015) demonstrated the existence of multiple-antibiotic-resistant bacterial strains from sites at Deception Island where human activity is commonly limited. A total of 43 isolates (out of 45) were resistant to at least three of the tested antibiotics, and 26 strains were resistant to 10 or more different antibiotics, with Pseudomonas spp. and four unknown Microbacteriaceae bacteria that were resistant to the majority of the tested antibiotics. All these findings proved evidence that Antarctic bacteria can act as potential reservoirs for antibiotic resistance genes and that, despite the precautions taken, no ecosystem is immune to human-driven alteration (Miller et al. 2009).

(Micro)plastics

Plastics are emerging contaminants mainly consisting of polyethene, polypropylene and polystyrene (typically used in packaging) (Hidalgo-Ruz et al. 2012). Plastic macroparticles (> 5 mm in size) break down to smaller particles, termed microplastics (5 mm–1 µm) and nanoplastics (< 1 µm), through a number of processes (e.g., photodegradation, physical abrasion, hydrolysis and biodegradation). Microplastic particles including personal care products (shampoos, toothpastes, shower gel) and fibres released from synthetic textiles enter the oceans via wastewater, representing the primary source of microplastic pollution. However, the majority of microplastics (both particles and fibers) in the marine environment are from secondary sources (i.e. the breakdown of macroplastics; Waller et al. 2017). The total degradation of plastics is very slow, especially at low temperatures, thus making them semi-persistent pollutants (Gewert et al. 2015). Evidences that plastic pollution affects polar areas are increasing in recent years, emphasizing the global relevance of this threat (Obbard 2018). Our current understanding of the distribution and transport of plastic litter and microplastics within Antarctic systems and of their potential effects on biota remains limited. Based on the annual human presence in the Antarctic continent, Waller et al. (2017) estimated plastic levels five times higher than expected. In the Antarctic continent, the occurrence of plastic objects (fishing buoys and plastic packaging pieces) in the Durmont D’Urville and Davis Seas as well as in the Amundsen Sea was first reported (Barnes et al. 2010). More recently, smaller plastic debris referable to microplastics were documented in surface waters (Cincinelli et al. 2017) and sediments (Van Cauwenberghe et al. 2013; Munari et al. 2017; Reed et al. 2018). While the impacts of plastics on the biota—and subsequently on public opinion—through, for example, entanglement and ingestion by marine predators and deposition of beached debris- are evident (Waller et al. 2017), microplastic pollution around Antarctica has received little scientific attention, and its extent and impacts in terms of their bioaccumulation, trophic transfer and toxicity on marine biota remain largely unknown (Reed et al. 2018). Plastic debris discharged as wastes from the Antarctic research bases could remain embedded in shallow and deep sea sediments, as well as within the cryosphere, but a fraction could be exchanged by hydrodynamic phenomena with the water column and carried through remote Antarctic areas with a dilution effect (Waller et al. 2017).

Plastics are themselves contaminants, but the plastic pollution problem is exacerbated by the fact that they could serve as a carrier for a number of other pollutants (including antibiotics, heavy metals and oily chemicals, such as pesticides and methylmercury), adsorbed on their surfaces. Plastics also constitute a novel and underexplored type of substrate for microbial colonization and transportation, including pathogenic and antibiotic-resistant bacteria (Caruso 2015).

Microbial assemblages on plastics, whose composition can change in relation to the synthetic polymers, show metabolic pathways and biogeochemical activities that are different from those of microbes in the surrounding environment (Bryant et al. 2016). Plastic-attached microbes could be also capable of degrading plastic polymers, resulting in the alteration of the buoyancy of polymers and the toxicity of plastics (Zettler et al. 2013; Reisser et al. 2014; Caruso 2015). In turn, the ability to degrade plastics by microorganisms, especially at low temperature, could lead to an environmental-friendly solution in mitigating plastic pollution in cold environments (Urbanek et al. 2018).

Except for few studies (Webster and Negri 2006; Lee et al. 2016), our knowledge on microbial colonization, and related larval settlements, on artificial substrates in extreme polar regions is still limited. Apart from a recent study on bacteria associated to the surface of polystyrene fragments recovered from King George Island (Laganà et al. 2018), proving that plastics could serve as a habitat for microbes that may express resistance to antibiotics, scientific knowledge on the transmission of antibiotic resistance in bacterial communities attached to plastics in Antarctic regions needs further understanding and research.

Concluding remarks

Despite of the precautionary measures to avoid pollution, the levels of many contaminant agents in the polar regions are likely to remain at or close to existing levels for decades. Much more efforts are necessary to better clarify the effects of individual or co-occurring contaminants on the unique and fragile Antarctic environment, and to find novel and suitable solutions to avoid and mitigate contamination events. In this regard, the bacterial communities not only strongly contribute to the functioning (e.g, driving biogeochemical cycles, sustaining key processes and producing energy) of the changing Antarctic coastal marine environment, but they may also represent the keystone for the environmental sustainability and restoration of Antarctic marine areas affected by local anthropogenic sources of contamination. The occurrence, function and ecology, and the biotechnology potential of bacterial communities inhabiting such a harsh environment have been investigated in the last decades. Microbes respond rapidly to the fluctuations of environmental parameters, and this is the reason why their response to changes deserves to be deeply researched upon. However, our current knowledge on the effects of climate change and/or other environmental perturbations on microbial population composition and eco-physiological activities is still at its infancy and derives from short-term and punctual investigations. But, what do we know about long-term consequences? Long-term monitoring of the structure, composition and activities of microbial communities might represent an excellent tool to check the state of the Antarctic environment. Further, analyzing the genetic and metabolic abilities of cold-adapted Antarctic bacteria can be useful for the development of bioremediation strategies and long-term previsions.

All the facets discussed in the above section claim for an interdisciplinary analysis of the risk assessment and environmental impact of the human presence in Antarctic. The synergistic interactions between chemists and microbiologists, studying several interconnected aspects, are becoming fundamental to preserve Antarctica.

Notes

Acknowledgements

This work was financially supported by PNRA (Programma Nazionale di Ricerche in Antartide) Grants (PNRA16_00020 and PNRA16_00105).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© Society for Environmental Sustainability 2019

Authors and Affiliations

  1. 1.Institute of Polar Sciences, National Research Council (ISP-CNR)MessinaItaly
  2. 2.Department of Chemical, Biological, Pharmacological and Environmental SciencesUniversity of MessinaMessinaItaly

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