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Review

The Virioneuston: A Review on Viral–Bacterial Associations at Air–Water Interfaces

by
Janina Rahlff
University of Duisburg-Essen, Biofilm Centre, Universitätsstraße 5, 45141 Essen, Germany
Viruses 2019, 11(2), 191; https://doi.org/10.3390/v11020191
Submission received: 29 January 2019 / Revised: 18 February 2019 / Accepted: 19 February 2019 / Published: 22 February 2019
(This article belongs to the Section Bacterial Viruses)
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Abstract

:
Vast biofilm-like habitats at air–water interfaces of marine and freshwater ecosystems harbor surface-dwelling microorganisms, which are commonly referred to as neuston. Viruses in the microlayer, i.e., the virioneuston, remain the most enigmatic biological entities in boundary surface layers due to their potential ecological impact on the microbial loop and major air–water exchange processes. To provide a broad picture of the viral–bacterial dynamics in surface microlayers, this review compiles insights on the challenges that viruses likely encounter at air–water interfaces. By considering viral abundance and morphology in surface microlayers, as well as dispersal and infection mechanisms as inferred from the relevant literature, this work highlights why studying the virioneuston in addition to the bacterioneuston is a worthwhile task. In this regard, major knowledge gaps and possible future research directions are discussed.

1. Introduction

Due to its exclusive position between the atmosphere and the hydrosphere and by spanning about 70% of the Earth’s surface, the sea-surface microlayer (sea-SML) is regarded as a fundamental component in air–sea exchange processes and in biogeochemical cycling [1]. Although having a minor thickness of <1000 µm [2], the elusive SML is long known for its distinct physicochemical characteristics compared to the underlying water [3], e.g., by featuring the accumulation of dissolved and particulate organic matter [3,4], transparent exopolymer particles (TEP), and surface-active molecules [5,6]. Therefore, the SML is a gelatinous biofilm [7], maintaining physical stability through surface tension forces [8]. It also forms a vast habitat for different organisms, collectively termed as neuston [9] with a recent global estimate of 2 × 1023 microbial cells for the sea-SML [10].
Life at air–water interfaces has never been considered easy, mainly because of the harsh environmental conditions that influence the SML [11]. However, high abundances of microorganisms, especially of bacteria and picophytoplankton, accumulating in the SML compared to the underlying water were frequently reported [4,12,13], accompanied by a predominant heterotrophic activity [14,15,16]. This is because primary production at the immediate air–water interface is often hindered by photoinhibition [17,18]. However, some exceptions of photosynthetic organisms, e.g., Trichodesmium, Synechococcus, or Sargassum, show more tolerance towards high light intensities and, hence, can become enriched in the SML [4,19,20]. Previous research has provided evidence that neustonic organisms can cope with wind and wave energy [12,21,22], solar and ultraviolet (UV) radiation [23,24,25], fluctuations in temperature and salinity [26,27], and a higher potential predation risk by the zooneuston [28]. Furthermore, wind action promoting sea spray formation and bubbles rising from deeper water and bursting at the surface release SML-associated microbes into the atmosphere [29]. In addition to being more concentrated compared to planktonic counterparts, the bacterioneuston, algae, and protists display distinctive community compositions compared to the underlying water, in both marine [8,19,20,21,30,31] and freshwater [32,33] habitats. Furthermore, the bacterial community composition was often dependent on the SML sampling device being used [34,35,36]. While being well defined with respect to bacterial community composition, little is known about viruses in the SML, i.e., the virioneuston. This review has its focus on virus–bacterium dynamics at air–water interfaces, even if viruses likely interact with other SML microbes, including archaea and the phytoneuston, as can be deduced from viral interference with their planktonic counterparts (reviewed by Brussaard [37] and Rohwer and Thurber [38]). Although viruses were briefly mentioned as pivotal SML components in a recent review on this unique habitat [39], a synopsis of the emerging knowledge and the major research gaps regarding bacteriophages at air–water interfaces is still missing in the literature.

2. Viruses as Overlooked Key Players in the SML Realm

Viruses are the most abundant biological entities in the water column of the world’s oceans [40]. Moreover, they are known as integral parts of global biogeochemical cycles [41], to shape and drive microbial diversity [42] and to structure trophic networks [43]. Like other neuston members, the virioneuston likely originates from the bulk seawater. For instance, Baylor et al. [44] postulated adsorption of viruses onto air bubbles as they rise to the surface [44], or viruses can stick to organic particles [45] also being transported to the SML via bubble scavenging [46].
Within the SML, viruses interacting with the bacterioneuston will probably induce the viral shunt, a phenomenon that is well known for marine pelagic systems. The term viral shunt describes the release of organic carbon and other nutritious compounds from the virus-mediated lysis of host cells, and its addition to the local dissolved organic matter (DOM) pool [47]. The enriched and densely packed bacterioneuston forms an excellent target for viruses compared to the bacterioplankton populating the subsurface. This is because high host-cell numbers will increase the probability of host–virus encounters. The viral shunt might effectively contribute to the SML’s already high DOM content enhancing bacterial production as previously suggested for pelagic ecosystems [43] and in turn replenishing host cells for viral infections (Figure 1). By affecting the DOM pool, viruses in the SML might directly interfere with the microbial loop being initiated when DOM is microbially recycled, converted into biomass, and passed along the food web. In addition, the release of DOM from lysed host cells by viruses contributes to organic particle generation [48]. However, the role of the virioneuston for the microbial loop has never been investigated.
Not only DOM but also organic particles show frequent enrichments within the SML [49], and Bigg et al. [50] reported that SML particles from the central Arctic Ocean were loaded with viruses. Van der Waals forces are responsible for the adsorption of phages to colloid materials [51], and Weinbauer et al. [52] suggested that aggregates could be net scavengers of attached viruses reducing the abundance of free-living ones [53]. Viruses were also found attached to TEPs along trophic gradients in the southwestern lagoon of New Caledonia [45]. The authors showed a positive correlation of TEP size and viral abundance, and further proposed TEPs being hot spots for viral infections [37]. Considering that unballasted TEPs can be highly enriched within the SML due to their lower density than seawater [13,54,55], studying the interactions between SML and TEPs and the virioneuston becomes highly relevant. Organic-particle aggregation and vertical transport may have crucial implications for carbon cycling and viral dispersal either by buoyant TEPs accumulating in the SML or by sinking TEPs falling to the deep sea.
Enrichment of surfactants in the SML was observed even at considerable high oceanic wind speeds up to ~13 m s−1 [56]. Surfactants can be either produced by phytoplankton [40] or marine bacteria [57]. Typical operational taxonomic units sequenced from the SML were assigned to Bacillus spp. or Acinetobacter spp. and were strongly associated with surfactants [58]. Interestingly, some surface-active agents produced by marine bacteria, such as pumilacidin, which is derived from Bacillus pumilus, possess antiviral properties [59]. The surfactant surfactin produced by Bacillus subtilis showed in vitro inactivation of a broad range of viruses and worked more efficiently against enveloped than non-enveloped ones [60]. The underlying mechanism includes the disruption of the viral lipid membrane and partially the capsid [60]. Since some water- and airborne viruses from the SML bear envelopes [61], they might become targets of surfactants. However, a deeper knowledge about virus–host–surfactant interactions is required to reveal if the SML could be a source for new powerful antiviral chemicals.
In sufficient quantities, surfactants can suppress air–sea gas exchange across the SML [62,63]. Consequently, enhanced viral lysis of bacterial and algal host cells would result in the release of more surfactants and nutrients from dead cells, and might be particularly profound for virus-mediated termination of large surface blooms [64]. The increase in organics enhances turnover and production of new bacteria including those able to actively produce surfactants. These processes could theoretically reinforce the gas-exchange suppressive effect exerted by surfactants and reduce gas transfer across the SML. Doubtlessly, this will be of particular importance for climate-relevant gases such as carbon dioxide, whose transfer across the air–sea boundary has a known dependency on biogenic surfactants [65]. The role of viruses on air–sea gas exchange by the induction of bacterial and algal surfactant release, due to increased mortality but also as a potential antiviral defense mechanism of living cells, has found no attention to date.
Furthermore, bacteria are often found in high abundances within slicks, which are visual surface films forming at calm sea states when high surfactant loads dampen the energy of small waves [66]. Wurl, Stolle, Van Thuoc, Thu, and Mari [13] found that slicks have a high microbial biomass and the bacterial community composition was different from the underlying water when compared to non-slick areas. Whether slicks also differ from non-slicky SML regarding their viral communities remains to be determined. At least, certain types of slicks were formerly linked to cyanobacterial blooms such as of Trichodesmium sp. [67,68] or Synechococcus sp. [14]. The presence of cyanobacterial slicks at the air–sea boundary might be in accordance with a recent mesocosm study where different Synechococcus and Prochlorococcus phages were observed in aerosols, SML, and bulk water [61].
Microorganisms additionally become enriched in patchy surface foams [69], essentially originating from wind-induced compression of the SML [70], as well as from rising bubbles that accumulate at the surface but do not burst instantaneously [71]. Whether viruses benefit from the increased microbial biomass enriched in slicks and foams by following the “kill-the-winner” theorem [72], i.e., infecting the most abundant prokaryotes and thus maintaining bacterial diversity, remains another yet-to-be-answered question. Effects on the prokaryotic community composition should be considered in this context.

3. Viral Abundance and Morphotypes in the SML

In the free water column, the virioplankton typically outnumbers the bacterioplankton by one order of magnitude reaching typical bulk water concentrations of 107 viruses mL−1 [41]. Research on the virioneuston is still in its infancy. The current body of literature shows that viruses, like their hosts, are sometimes enriched in the SML over underlying water (Table 1), though results are overall inconclusive. This may be because sampled bulk water depths varied considerably between studies (0.15–20 m), and sampling of viruses from the neuston has been conducted with a range of sampling devices (Table 1). The glass-plate sampler and the mesh screen were both regarded as suitable tools for virus sampling [35], but more comparative studies for the various types of sampling methods and with a focus on virus sampling would be desirable.
A study by Tapper and Hicks [73] found a viral abundance range of 0.1–9 × 106 viruses mL−1 for Lake Superior (North America) with 2–15 times more viruses occurring in the upper 20 µm layer compared to water from 20 m beneath the surface. Joux et al. [74] studied the enrichment of virus-like particles (VLPs) at two coastal sites in the northwestern Mediterranean Sea and found contrasting results for enrichment factors (EF)—defined as the ratio of a species’ concentration in the SML relative to its concentration in the underlying water [75]. The EF of VLPs was close to 1 (no enrichment) at both sites during three sampling time points except for one time point, where an EF of 5.1 was recorded. Absolute counts of VLPs were in a range of 0.3–204 × 106 viruses mL−1 as determined by VLP enumeration under the microscope. Likewise, Kuznetsova et al. [76] reported slight enrichments of VLPs for the SML (EF on average ~1.5), and VLP concentrations in the range of 1–10 × 106 viruses mL−1 along a transect from coastal Massachusetts to the open ocean waters of the Sargasso Sea (Table 1). A highly significant, positive correlation between viral abundance in the SML and the underlying water from the various studies shown in Table 1 (Spearman rank correlation coefficient rs = 0.825, two-tailed analysis: p < 0.0001, n = 44) possibly supports the previous assumption of SML viruses originating from the underlying bulk water.
However, correlations between viral and host abundance in the SML were not apparent [74,76] as formerly shown for marine pelagic systems [77]. Probably environmental factors and/or the bacterial community composition drive the prevailing virus–host dynamics. The virus to bacteria ratio was previously shown to be ~10-fold higher in freshwater than in marine environments [78], but due to the limited amount of data, more work is certainly needed to confirm these trends for the SML. According to field data from previous studies (Table 1), virus to bacteria ratios ranged from 0.1 to 139 (median = 1.5) and from 0.03 to 29 (median = 1.8) in the SML and underlying water, respectively. Data from the mesocosm study [61] were excluded from this calculation as SML bacterial cell counts often reach unusually large numbers in artificial experimental setups [79] and, hence, might not be representative. The median values illustrate that viruses were only slightly more abundant than bacteria in both SML and subsurface if primarily marine samples were considered. A speculative reason for this observation could be that most viruses, despite relatively high bacterial numbers, reside in a non-infectious state within host cells and hence follow a strategy known as “piggyback the winner” [80] contrasting the “kill-the-winner” theorem [72]. Likewise, the harsh environmental conditions at the air–sea boundary could effectively prevent a switch to the lytic cycle. However, according to the calculated ratio, the same theory would then apply for the slightly deeper surface water. Another explanation could be that only certain viruses can tolerate SML conditions, and that they have a very narrow host range. An infection of only certain, perhaps, low-abundant host strains would also prevent viruses from reaching high numbers. Thus, to fully understand the underlying viral–bacterial dynamics, the virioneuston should best be analyzed together with the host-community composition.
The usual size range of marine viral particles ranges between 20 and 200 nm [41]. In one study, smaller particles between 20 and 60 nm were reported for virioneuston members of the central Arctic Ocean in summer 2001 [50]. Studies on the role of environmental factors such as high solar irradiance on VLP size in the SML would be useful but do not exist so far. Tapper and Hicks [73] found that about 70% of the total free viruses in the SML and subsurface water from Lake Superior were tailed by using transmission electron microscopy (TEM). The typical (polyhedral) head and tail morphology of the free viruses led the authors to assume that the viruses were bacteriophages. Head sizes were in the range of 10–70 nm, tails ranged from 10 to 110 nm. Most free viruses had a head size <60 nm and a tail. Based on TEM observations on SML samples, Ram et al. [81] found that the SML of a tropical coastal ecosystem was dominated by myoviruses (42%), which include bacteriophages possessing a contractile tail and broad host ranges [82]. Also, metagenomic sequencing revealed tailed bacteriophages of the Caudovirales (including Myoviridae and Podoviridae) in the SML in a mesocosm study [61]. Whether the viral morphologies fulfill an adaptive function for the virioneuston to inhabit in the SML or benefit interference with a particular host type requires more research on the structural features of different virioneuston members.
Table
Table 1. Bacterial and viral abundances and ratios in the surface microlayer (SML) and underlying water (ULW). If n > 1, either ranges of minimum to maximum values are given in parentheses or ± standard deviation obtained from the reference source. EF = enrichment factor.
Table 1. Bacterial and viral abundances and ratios in the surface microlayer (SML) and underlying water (ULW). If n > 1, either ranges of minimum to maximum values are given in parentheses or ± standard deviation obtained from the reference source. EF = enrichment factor.
Viral Abundance (×106 mL−1)EFnBacterial Abundance (×106 cells mL−1)EFnVirus to Bacteria RatioSampling SiteSML Sampling DeviceULW Depth (m)Reference
SMLULWSML/ULWSMLULWSML/ULWSMLULW
13.2 ± 1.916.8 ± 3.20.838.6 ± 0.0187.3 ± 0.101.231.52.3Mesocosm experiment, day 7 (Pacific seawater)Glass plate0.9[61]
12.1 ± 2.26.0 ± 1.02.039.6 ± 0.0159.9 ± 0.061.031.30.6Mesocosm experiment, day 8 (Pacific seawater)Glass plate0.9[61]
12.1 ± 2.219.3 ± 2.10.639.8 ± 0.0818.8 ± 0.121.131.22.2Mesocosm experiment, day 9 (Pacific seawater)Glass plate0.9[61]
14.3 ± 2.811.0 ± 3.81.3311.7 ± 0.1110.0 ± 0.0511.231.21.1Mesocosm experiment, day 10 (Pacific seawater)Glass plate0.9[61]
20.8 ± 2.729.9 ± 3.60.737.2 ± 0.01510.0 ± 0.0150.732.13.0Mesocosm experiment, day 16 (Pacific seawater)Glass plate0.9[61]
35.4 ± 4.223.6 ± 2.61.5310.9 ± 0.179.8 ± 0.311.133.22.4Mesocosm experiment, day 17 (Pacific seawater)Glass plate0.9[61]
38.5 ± 5.129.1 ± 4.21.3312.0 ± 0.3511.0 ± 0.241.133.22.6Mesocosm experiment, day 18 (Pacific seawater)Glass plate0.9[61]
39.0 ± 4.243.6 ± 3.60.938.6 ± 0.0718.4 ± 0.121.034.55.2Mesocosm experiment, day 21 (Pacific seawater)Glass plate0.9[61]
30.4 ± 4.379.7 ± 7.90.4314.7 ± 0.09112.4 ± 0.441.232.16.4Mesocosm experiment, day 22 (Pacific seawater)Glass plate0.9[61]
36.6 ± 3.547.6 ± 6.50.8333.5 ± 0.2618.6 ± 0.751.831.12.6Mesocosm experiment, day 23 (Pacific seawater)Glass plate0.9[61]
39.6 ± 5.336.3 ± 5.21.1333.3 ± 0.03929.8 ± 1.271.131.21.2Mesocosm experiment, day 24 (Pacific seawater)Glass plate0.9[61]
7.3 (4.1–18.4)3.1 (2.0–4.9)2.4161.3 (0.5–2.9)0.6 (0.5–1.0)2.2166.45.0Halong Bay, Vietnam, Oct. 2012Glass plate1.5[81]
125 (46–204)25 (24–26)5.120.9 (0.9–0.9)0.9 (1.0–0.9)1.02138.927.8Mediterranean Sea, Barcelona Site, Sept. 2001Metal screen0.5[74]
1.8 (1.0–2.5)1.6 (1.1–2.1)1.122.6 (1.7–4.0)2.4 (1.3–3.9)1.220.70.7Mediterranean Sea, Barcelona Site, Mar. 2002Metal screen0.5[74]
24.525.80.911.0 (0.9–1.1)0.9 (0.9–1.0)1.1224.528.7Mediterranean Sea, Banyuls Site, Sept. 2001Metal screen0.5[74]
0.4 (0.3–0.4)0.3 (0.3–0.4)1.130.9 (0.8–1.2)1.0 (0.8–1.1)0.930.40.3Mediterranean Sea, Banyuls Site, Mar. 2002Metal screen0.5[74]
10.91.47.8112.46.22.010.90.2Stony Brook Harbor, NY, June 2003Polyester screen0.15[83]
2.43.10.812.01.71.211.21.8Stony Brook Harbor, NY, July 2003Polyester screen0.15[83]
2.40.92.712.71.61.710.90.6North Atlantic Ocean, Sample No. 1, June 2001Polyester screen0.15[76]
1.91.71.111.91.51.211.31.1North Atlantic Ocean, Sample No. 2, June 2001Polyester screen0.15[76]
2.83.90.711.61.51.111.52.7North Atlantic Ocean, Sample No. 3, June 2001Polyester screen0.15[76]
5.52.91.912.01.81.111.21.6North Atlantic Ocean, Sample No. 4, June 2001Rotating drum0.15[76]
1.61.01.611.01.10.912.40.9North Atlantic Ocean, Sample No. 5, June 2001Polyester screen0.15[76]
4.62.22.011.30.71.711.93.1North Atlantic Ocean, Sample No. 6, June 2001Polyester screen0.15[76]
3.01.22.410.70.61.113.62.0North Atlantic Ocean, Sample No. 7, June 2001Polyester screen0.15[76]
2.42.01.210.70.61.213.53.4North Atlantic Ocean, Sample No. 8, June 2001Polyester screen0.15[76]
2.52.41.011.20.81.512.13.1North Atlantic Ocean, Sample No. 9, June 2001Polyester screen0.15[76]
3.22.81.210.91.00.912.72.7North Atlantic Ocean, Sample No. 10, June 2001Rotating drum0.15[76]
3.14.10.811.30.91.411.94.5North Atlantic Ocean, Sample No. 11, June 2001Polyester screen0.15[76]
3.83.91.011.00.81.212.54.9North Atlantic Ocean, Sample No. 12, June 2001Polyester screen0.15[76]
2.33.50.710.70.80.913.44.5North Atlantic Ocean, Sample No. 14, June 2001Rotating drum0.15[76]
6.93.81.811.30.91.511.94.5North Atlantic Ocean, Sample No. 15, June 2001Polyester screen0.15[76]
3.83.41.112.20.92.311.13.7North Atlantic Ocean, Sample No. 16, June 2001Polyester screen0.15[76]
1.91.71.111.31.21.111.91.4North Atlantic Ocean, Sample No. 17, June 2001Rotating drum0.15[76]
2.81.71.711.91.31.411.31.3North Atlantic Ocean, Sample No. 18, June 2001Polyester screen0.15[76]
3.53.21.111.21.01.212.03.3North Atlantic Ocean, Sample No. 19, June 2001Polyester screen0.15[76]
2.72.01.411.51.41.111.61.5North Atlantic Ocean, Sample No. 20, June 2001Rotating drum0.15[76]
10.95.12.112.41.71.411.03.1North Atlantic Ocean, Sample No. 21, June 2001Polyester screen0.15[76]
1.71.01.712.61.91.410.90.5North Atlantic Ocean, Sample No. 22, June 2001Rotating drum0.15[76]
3.12.01.512.41.71.411.01.2North Atlantic Ocean, Sample No. 23, June 2001Polyester screen0.15[76]
2.80.215.415.22.22.310.50.1Lake Superior, June 1993Teflon sheet20[73]
9.20.910.7118.31.215.410.10.7Lake Superior, July 1993Teflon sheet20[73]
0.70.32.211.71.70.911.50.2Lake Superior, Aug. 1993Teflon sheet20[73]
1.70.211.019.24.62.010.30.03Lake Superior, Oct. 1993Teflon sheet20[73]

4. Viral Dispersal in and out of the SML

While it was shown that bacteria are actively transferred from bursting bubbles at the sea surface to sea-spray aerosols [84], the same is obviously true for viruses [44,83,85], which can even end up in clouds [86] (Figure 1). In one recent study, virus aerosolization was proposed to be less efficient than for bacteria [61]. This is because viral concentrations in aerosols were very similar to those of bacteria (1.19 × 107 ± 0.58 × 107 cells m−3), i.e., bacteria were preferentially aerosolized over viruses, or viruses were more prone to decay. Considering that aerosols originate from SML material, the observation of equal numbers of bacteria and viruses in aerosols also matches my previous calculation showing that virus to bacteria ratios expressed as a median over several field studies were in the same range for both SML and underlying water. However, there is also contradictory evidence claiming that more viruses than prokaryotes occur in experimentally produced aerosols [87]. Apparently, more conclusive work is needed on the topic.
As inferred from genomic comparisons, lipid-enveloped viruses such as Polydnaviridae and Alloherpesviridae got airborne suggesting that hydrophobic surfaces are crucial for this process [61]. This is in line with another report finding 140,000-fold enrichments of lipids in experimentally produced aerosols compared to seawater, which the authors attributed to the surface-active properties of lipids [87]. Thus, morphological characteristics could be equally important for governing virus aerosolization as environmental factors. Atmospheric transport of viruses might be an important dispersal mechanism for spreading viral infections over long distances over the ocean [88]. Interestingly, Reche et al. showed that viruses are associated with smaller aerosol particles compared to bacteria, which prolongs their atmospheric residence time [89] providing a sound explanation for the fact that identical viral sequences can occur in geographically distant environments [90,91]. While the existence of potentially pathogenic bacterial strains such as of Legionella and Vibrio in surface films has been reported [8,22,61], a potential threat for public health by the presence of pathogenic viruses and their dispersal from the SML still needs to be elucidated.
In addition, viruses were found attached to mesozooplankton, e.g., collected from the neuston of the Red Sea using a Manta neuston net that sampled the top 1 m of the water column [92]. Due to observed high mortality of copepods (phylum Arthropoda) in their samples, the authors were looking for VLPs on Acartia fossae, a blue-pigmented surface-dwelling copepod, and its prey, Trichodesmium cells. Analyses using TEM revealed different morphologies of VLPs on the copepods in contrast to the Trichodesmium cells. Metatranscriptomic analyses showed that genes responsive to virus reproduction showed increased expression in these copepods. Therefore, this study provided a first important indication for the interaction between viruses and higher, non-prokaryotic trophic levels. This aspect deserves further investigation, as many mesozooplankton species frequently populate the SML [4,93] and hence represent appropriate bacterial and viral targets. Zooplankton species that occasionally migrate to the SML during diel vertical migration or for feeding purposes [28] might also serve as important vectors for viruses that infect bacteria or phytoplankton living therein [94] (Figure 1).

5. Infection Mechanisms of the Virioneuston

Most marine viruses in surface water are infective [95], but contradictory assumptions exist on the prevailing viral infection mode for the SML. On the one hand, due to the stressful environmental conditions associated with populating the SML [11], lysogeny as a survival mechanism might be the preferred viral infection strategy [73]. The extent of lysogeny, i.e., the integration of the viral genome (the prophage) into the host genome, can be experimentally estimated by induction of prophages into lytic phages using UV radiation or the antibiotic mitomycin C [96]. Tapper and Hicks [73] reported on higher amounts of temperate prophages in the SML (0.1%–7.4%) compared to the underlying water (0.1%–1.8%) in freshwater.
On the other hand, the high incidence of UV radiation at the immediate air–sea interface could induce prophages to become lytic, even though natural UV light was not always efficient to induce lysogens in surface water [97]. A range of other important environmental conditions such as sudden changes in temperature or the effect of pollutants (mainly of polyaromatic hydrocarbons, PAHs) can induce lysogenic viral production as previously demonstrated for marine and estuarine environments [98]. Since the SML is a repository for PAHs and prone to temperature fluctuations [3,99], these inducing agents may have particular relevance for prophage induction in this habitat.
High host abundance and system productivity can promote the lytic lifestyle of viruses [100]. In one case when bacterial production in the SML of Halong Bay, Vietnam was higher than in the underlying water, viral lytic infections (5.3%–30.1%) dominated over lysogeny (0%–1.4%). The same study demonstrated that certain bacterial morphotypes, namely rod-shaped cells, were particularly prone to viral lysis [81]. Since certain bacteria stick to organic particles within the SML [49], virally infected bacteria attached to particles might be masked and hard to find using microscopic approaches [81], a fact that should be considered in future virioneuston studies focusing on the detection of lytic behavior.

6. Future Perspectives and Conclusions

Recent advances in viral metagenomics (viromics) allow for high-throughput sequencing approaches and in silico detection of novel viruses from uncultured environmental samples. New bioinformatic tools for the identification of viral genomes based on major hallmark genes [101] and k-mer frequencies [102] and for matching hosts to viruses [103] have largely facilitated this progress (recent review by Hurwitz et al. [104]). In addition, an improved understanding on the role of clustered regularly interspaced short palindromic repeats (CRISPR) as a prokaryotic viral defense mechanism allows microbiologists to link viruses to their hosts by matching viral protospacers to host CRISPR spacers [105]. Unfortunately, only one single study used metagenomic sequencing to explore viral and bacterial communities in the SML, underlying water, and aerosol samples in a mesocosm setup [61]. More work is needed to identify which major environmental factors (turbulence resulting from wind speed, solar radiation, temperature, etc.) dominantly shape the virioneuston community and whether these influences are independent from the host community. Elucidating the major viral infection strategies during different environmental conditions, from different seasons, and latitudes, remains another open task to be addressed. Viral impacts on surfactant release and surface blooms implement influences on gas exchange and biogeochemical matter cycling and require further attention. Dispersal of airborne viruses originating from the SML, and potential hazards for the public should get more into our focus.
Air–water interfaces span more than 70% of the global surface area and therein sojourning viruses likely have profound implications for biogeochemical cycling, gas exchange, food web structure, and human health. This review illustrates that much more remains to be discovered about how the virioneuston copes with the many challenges caused by its unorthodox position between the lower atmosphere and the upper hydrosphere.

Funding

This research received no external funding.

Acknowledgments

I would like to thank my colleagues Christian Stolle, Mara Elena Heinrichs, and Katharina Melkonian for their valuable feedback on this manuscript. I further acknowledge support by the Open Access Publication Fund of the University of Duisburg-Essen.

Conflicts of Interest

The author declares no conflict of interest.

References

  1. Cunliffe, M.; Engel, A.; Frka, S.; Gašparović, B.; Guitart, C.; Murrell, J.C.; Salter, M.; Stolle, C.; Upstill-Goddard, R.; Wurl, O. Sea surface microlayers: A unified physicochemical and biological perspective of the air–ocean interface. Progr. Oceanogr. 2013, 109, 104–116. [Google Scholar] [CrossRef]
  2. Liss, P.S.; Duce, R.A. The Sea Surface and Global Change; Cambridge University Press: Cambridge, UK, 1997. [Google Scholar]
  3. Hardy, J.T. The sea surface microlayer: Biology, chemistry and anthropogenic enrichment. Progr. Oceanogr. 1982, 11, 307–328. [Google Scholar] [CrossRef]
  4. Sieburth, J.M.; Willis, P.J.; Johnson, K.M.; Burney, C.M.; Lavoie, D.M.; Hinga, K.R.; Caron, D.A.; French, F.W., 3rd; Johnson, P.W.; Davis, P.G. Dissolved organic matter and heterotrophic microneuston in the surface microlayers of the North Atlantic. Science 1976, 194, 1415–1418. [Google Scholar] [CrossRef] [PubMed]
  5. Wurl, O.; Miller, L.; Ruttgers, R.; Vagle, S. The distribution and fate of surface-active substances in the sea-surface microlayer and water column. Mar. Chem. 2009, 115, 1–9. [Google Scholar] [CrossRef]
  6. Wurl, O.; Holmes, M. The gelatinous nature of the sea-surface microlayer. Mar. Chem. 2008, 110, 89–97. [Google Scholar] [CrossRef]
  7. Cunliffe, M.; Murrell, J.C. The sea-surface microlayer is a gelatinous biofilm. ISME J. 2009, 3, 1001–1003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Franklin, M.P.; McDonald, I.R.; Bourne, D.G.; Owens, N.J.; Upstill-Goddard, R.C.; Murrell, J.C. Bacterial diversity in the bacterioneuston (sea surface microlayer): The bacterioneuston through the looking glass. Environ. Microbiol. 2005, 7, 723–736. [Google Scholar] [CrossRef] [PubMed]
  9. Naumann, E. Beiträge zur Kenntnis des Teichnannoplanktons, II. Über das Neuston des Süsswassers. Biol. Centralblatt 1917, 37, 98–106. [Google Scholar]
  10. Flemming, H.C.; Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 2019. [Google Scholar] [CrossRef] [PubMed]
  11. Maki, J. The air-water interface as an extreme environment. In Aquatic Microbiology: An Ecological Approach; Ford, T., Ed.; Blackwell Scientific Publication: Boston, MA, USA, 1993; pp. 409–439. [Google Scholar]
  12. Tsyban, A. Marine bacterioneuston. J. Oceanogr. Soc. Jpn. 1971, 27, 56–66. [Google Scholar] [CrossRef]
  13. Wurl, O.; Stolle, C.; Van Thuoc, C.; Thu, P.T.; Mari, X. Biofilm-like properties of the sea surface and predicted effects on air-sea CO2 exchange. Progr. Oceanogr. 2016, 144, 15–24. [Google Scholar] [CrossRef]
  14. Obernosterer, I.; Catala, P.; Reinthaler, T.; Herndl, G.J.; Lebaron, P. Enhanced heterotrophic activity in the surface microlayer of the Mediterranean Sea. Aquat. Microb. Ecol. 2005, 39, 293–302. [Google Scholar] [CrossRef] [Green Version]
  15. Reinthaler, T.; Sintes, E.; Herndl, G.J. Dissolved organic matter and bacterial production and respiration in the sea-surface microlayer of the open Atlantic and the western Mediterranean Sea. Limnol. Oceanogr. 2008, 53, 122–136. [Google Scholar] [CrossRef] [Green Version]
  16. Rahlff, J.; Stolle, C.; Wurl, O. SISI: A new device for in situ incubations at the ocean surface. J. Mar. Sci. Eng. 2017, 5, 46. [Google Scholar] [CrossRef]
  17. Williams, P.M.; Carlucci, A.F.; Henrichs, S.M.; Van Vleet, E.S.; Horrigan, S.G.; Reid, F.M.H.; Robertson, K.J. Chemical and microbiological studies of sea-surface films in the Southern Gulf of California and off the west coast of Baja California. Mar. Chem. 1986, 19, 17–98. [Google Scholar] [CrossRef]
  18. Albright, L.J. Photosynthetic activities of phytoneuston and phytoplankton. Can. J. Microbiol. 1980, 26, 389–392. [Google Scholar] [CrossRef]
  19. Yue, W.Z.; Sun, C.C.; Shi, P.; Engel, A.; Wang, Y.S.; He, W.H. Effect of temperature on the accumulation of marine biogenic gels in the surface microlayer near the outlet of nuclear power plants and adjacent areas in the Daya Bay, China. PLoS ONE 2018, 13, e0198735. [Google Scholar] [CrossRef]
  20. Hardy, J.T.; Coley, J.A.; Antrim, L.D.; Kiesser, S.L. A hydrophobic large-volume sampler for collecting aquatic surface microlayers: Characterization and comparison with the glass plate method. Can. J. Fish. Aquat. Sci. 1988, 45, 822–826. [Google Scholar] [CrossRef]
  21. Stolle, C.; Labrenz, M.; Meeske, C.; Jürgens, K. Bacterioneuston community structure in the southern Baltic Sea and its dependence on meteorological conditions. Appl. Environ. Microbiol. 2011, 77, 3726–3733. [Google Scholar] [CrossRef]
  22. Rahlff, J.; Stolle, C.; Giebel, H.A.; Brinkhoff, T.; Ribas-Ribas, M.; Hodapp, D.; Wurl, O. High wind speeds prevent formation of a distinct bacterioneuston community in the sea-surface microlayer. FEMS Microbiol. Ecol. 2017, 93. [Google Scholar] [CrossRef] [Green Version]
  23. Santos, A.L.; Lopes, S.; Baptista, I.; Henriques, I.; Gomes, N.C.; Almeida, A.; Correia, A.; Cunha, A. Diversity in UV sensitivity and recovery potential among bacterioneuston and bacterioplankton isolates. Lett. Appl. Microbiol. 2011, 52, 360–366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Agogué, H.; Joux, F.; Obernosterer, I.; Lebaron, P. Resistance of marine bacterioneuston to solar radiation. Appl. Environ. Microbiol. 2005, 71, 5282–5289. [Google Scholar] [CrossRef] [PubMed]
  25. Santos, A.L.; Oliveira, V.; Baptista, I.; Henriques, I.; Gomes, N.C.; Almeida, A.; Correia, A.; Cunha, A. Effects of UV-B radiation on the structural and physiological diversity of bacterioneuston and bacterioplankton. Appl. Environ. Microbiol. 2012, 78, 2066–2069. [Google Scholar] [CrossRef] [PubMed]
  26. Hardy, J.T. Phytoneuston ecology of a temperate marine lagoon. Limnol. Oceanogr. 1973, 18, 525–533. [Google Scholar] [CrossRef] [Green Version]
  27. Norkrans, B. Surface microlayers in aquatic environments. In Advances in Microbial Ecology; Alexander, M., Ed.; Springer: Boston, MA, USA, 1980; Volume 4, pp. 51–85. [Google Scholar]
  28. Rahlff, J.; Ribas-Ribas, M.; Brown, S.M.; Mustaffa, N.I.H.; Renz, J.; Peck, M.A.; Bird, K.; Cunliffe, M.; Melkonian, K.; Zappa, C.J. Blue pigmentation of neustonic copepods benefits exploitation of a prey-rich niche at the air-sea boundary. Sci. Rep. 2018, 8, 11510. [Google Scholar] [CrossRef]
  29. Blanchard, D.C. The ejection of drops from the sea and their enrichment with bacteria and other materials: A review. Estuaries Coasts 1989, 12, 127–137. [Google Scholar] [CrossRef]
  30. Cunliffe, M.; Whiteley, A.S.; Newbold, L.; Oliver, A.; Schäfer, H.; Murrell, J.C. Comparison of bacterioneuston and bacterioplankton dynamics during a phytoplankton bloom in a fjord mesocosm. Appl. Environ. Microbiol. 2009, 75, 7173–7181. [Google Scholar] [CrossRef]
  31. Cunliffe, M.; Murrell, J.C. Eukarya 18S rRNA gene diversity in the sea surface microlayer: Implications for the structure of the neustonic microbial loop. ISME J. 2010, 4, 455–458. [Google Scholar] [CrossRef]
  32. Hugoni, M.; Vellet, A.; Debroas, D. Unique and highly variable bacterial communities inhabiting the surface microlayer of an oligotrophic lake. Aquat. Microb. Ecol. 2017, 79, 115–125. [Google Scholar] [CrossRef]
  33. Hörtnagl, P.; Perez, M.T.; Zeder, M.; Sommaruga, R. The bacterial community composition of the surface microlayer in a high mountain lake. FEMS Microbiol. Ecol. 2010, 73, 458–467. [Google Scholar] [CrossRef]
  34. Stolle, C.; Nagel, K.; Labrenz, M.; Jürgens, K. Bacterial activity in the sea-surface microlayer: In situ investigations in the Baltic sea and the influence of sampling devices. Aquat. Microb. Ecol. 2009, 58, 67–78. [Google Scholar] [CrossRef]
  35. Agogué, H.; Casamayor, E.O.; Joux, F.; Obernosterer, I.; Dupuy, C.; Lantoine, F.; Catala, P.; Weinbauer, M.G.; Reinthaler, T.; Herndl, G.J.; et al. Comparison of samplers for the biological characterization of the sea surface microlayer. Limnol. Oceanogr.-Meth. 2004, 2, 213–225. [Google Scholar] [CrossRef] [Green Version]
  36. Cunliffe, M.; Harrison, E.; Salter, M.; Schäfer, H.; Upstill-Goddard, R.C.; Murrell, J.C. Comparison and validation of sampling strategies for the molecular microbial analysis of surface microlayers. Aquat. Microb. Ecol. 2009, 57, 69–77. [Google Scholar] [CrossRef] [Green Version]
  37. Brussaard, C.P. Viral control of phytoplankton populations—A review. J. Eukaryot. Microbiol. 2004, 51, 125–138. [Google Scholar] [CrossRef]
  38. Rohwer, F.; Thurber, R.V. Viruses manipulate the marine environment. Nature 2009, 459, 207–212. [Google Scholar] [CrossRef]
  39. Engel, A.; Bange, H.W.; Cunliffe, M.; Burrows, S.M.; Friedrichs, G.; Galgani, L.; Herrmann, H.; Hertkorn, N.; Johnson, M.; Liss, P.S.; et al. The ocean’s vital skin: Toward an integrated understanding of the sea surface microlayer. Front. Mar. Sci. 2017, 4. [Google Scholar] [CrossRef]
  40. Suttle, C.A. Viruses in the sea. Nature 2005, 437, 356–361. [Google Scholar] [CrossRef]
  41. Fuhrman, J.A. Marine viruses and their biogeochemical and ecological effects. Nature 1999, 399, 541. [Google Scholar] [CrossRef]
  42. Weinbauer, M.G.; Rassoulzadegan, F. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 2004, 6, 1–11. [Google Scholar] [CrossRef]
  43. Thingstad, T.F.; Heldal, M.; Bratbak, G.; Dundas, I. Are viruses important partners in pelagic food webs? Trends Ecol. Evol. 1993, 8, 209–213. [Google Scholar] [CrossRef]
  44. Baylor, E.; Baylor, M.; Blanchard, D.C.; Syzdek, L.D.; Appel, C. Virus transfer from surf to wind. Science 1977, 198, 575–580. [Google Scholar] [CrossRef] [PubMed]
  45. Mari, X.; Kerros, M.E.; Weinbauer, M.G. Virus attachment to transparent exopolymeric particles along trophic gradients in the southwestern lagoon of New Caledonia. Appl. Environ. Microbiol. 2007, 73, 5245–5252. [Google Scholar] [CrossRef] [PubMed]
  46. Wilson, T.W.; Ladino, L.A.; Alpert, P.A.; Breckels, M.N.; Brooks, I.M.; Browse, J.; Burrows, S.M.; Carslaw, K.S.; Huffman, J.A.; Judd, C.; et al. A marine biogenic source of atmospheric ice-nucleating particles. Nature 2015, 525, 234–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Wilhelm, S.W.; Suttle, C.A. Viruses and nutrient cycles in the sea: Viruses play critical roles in the structure and function of aquatic food webs. Bioscience 1999, 49, 781–788. [Google Scholar] [CrossRef]
  48. Wells, M.L.; Goldberg, E.D. Marine submicron particles. Mar. Chem. 1992, 40, 5–18. [Google Scholar] [CrossRef]
  49. Alldredge, A.L.; Passow, U.; Logan, B.E. The abundance and significance of a class of large, transparent organic particles in the ocean. Deep Sea Res. Part I Oceanogr. Res. Pap. 1993, 40, 1131–1140. [Google Scholar] [CrossRef]
  50. Bigg, E.K.; Leck, C.; Tranvik, L. Particulates of the surface microlayer of open water in the central Arctic Ocean in summer. Mar. Chem. 2004, 91, 131–141. [Google Scholar] [CrossRef]
  51. Chattopadhyay, S.; Puls, R.W. Forces dictating colloidal interactions between viruses and soil. Chemosphere 2000, 41, 1279–1286. [Google Scholar] [CrossRef]
  52. Weinbauer, M.G.; Bettarel, Y.; Cattaneo, R.; Luef, B.; Maier, C.; Motegi, C.; Peduzzi, P.; Mari, X. Viral ecology of organic and inorganic particles in aquatic systems: Avenues for further research. Aquat. Microb. Ecol. 2009, 57, 321–341. [Google Scholar] [CrossRef]
  53. Peduzzi, P.; Luef, B. Viruses, bacteria and suspended particles in a backwater and main channel site of the Danube (Austria). Aquat. Sci. 2008, 70, 186–194. [Google Scholar] [CrossRef] [Green Version]
  54. Wurl, O.; Miller, L.; Vagle, S. Production and fate of transparent exopolymer particles in the ocean. J. Geophys. Res.-Oceans 2011, 116. [Google Scholar] [CrossRef] [Green Version]
  55. Mari, X.; Passow, U.; Migon, C.; Burd, A.B.; Legendre, L. Transparent exopolymer particles: Effects on carbon cycling in the ocean. Progr. Oceanogr. 2017, 151, 13–37. [Google Scholar] [CrossRef]
  56. Sabbaghzadeh, B.; Upstill-Goddard, R.C.; Beale, R.; Pereira, R.; Nightingale, P.D. The Atlantic Ocean surface microlayer from 50°N to 50°S is ubiquitously enriched in surfactants at wind speeds up to 13 m s−1. Geophys. Res. Lett. 2017, 44, 2852–2858. [Google Scholar] [CrossRef]
  57. Satpute, S.K.; Banat, I.M.; Dhakephalkar, P.K.; Banpurkar, A.G.; Chopade, B.A. Biosurfactants, bioemulsifiers and exopolysaccharides from marine microorganisms. Biotechnol. Adv. 2010, 28, 436–450. [Google Scholar] [CrossRef] [PubMed]
  58. Kurata, N.; Vella, K.; Hamilton, B.; Shivji, M.; Soloviev, A.; Matt, S.; Tartar, A.; Perrie, W. Surfactant-associated bacteria in the near-surface layer of the ocean. Sci. Rep. 2016, 6, 19123. [Google Scholar] [CrossRef] [Green Version]
  59. Naruse, N.; Tenmyo, O.; Kobaru, S.; Kamei, H.; Miyaki, T.; Konishi, M.; Oki, T. Pumilacidin, a complex of new antiviral antibiotics. Production, isolation, chemical properties, structure and biological activity. J. Antibiot. 1990, 43, 267–280. [Google Scholar] [CrossRef] [PubMed]
  60. Vollenbroich, D.; Ozel, M.; Vater, J.; Kamp, R.M.; Pauli, G. Mechanism of inactivation of enveloped viruses by the biosurfactant surfactin from Bacillus subtilis. Biologicals 1997, 25, 289–297. [Google Scholar] [CrossRef]
  61. Michaud, J.M.; Thompson, L.R.; Kaul, D.; Espinoza, J.L.; Richter, R.A.; Xu, Z.Z.; Lee, C.; Pham, K.M.; Beall, C.M.; Malfatti, F.; et al. Taxon-specific aerosolization of bacteria and viruses in an experimental ocean-atmosphere mesocosm. Nat. Commun. 2018, 9, 2017. [Google Scholar] [CrossRef] [PubMed]
  62. Frew, N.M.; Goldman, J.C.; Dennett, M.R.; Johnson, A.S. Impact of phytoplankton-generated surfactants on air-sea gas exchange. J. Geophys. Res.-Oceans 1990, 95, 3337–3352. [Google Scholar] [CrossRef]
  63. Goldman, J.C.; Dennett, M.R.; Frew, N.M. Surfactant effects on air-sea gas exchange under turbulent conditions. Deep Sea Res. Part I Oceanogr. Res. Pap. 1988, 35, 1953–1970. [Google Scholar] [CrossRef]
  64. Bratbak, G.; Egge, J.K.; Heldal, M. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 1993, 93, 39–48. [Google Scholar] [CrossRef]
  65. Pereira, R.; Ashton, I.; Sabbaghzadeh, B.; Shutler, J.D.; Upstill-Goddard, R.C. Reduced air–sea CO2 exchange in the atlantic ocean due to biological surfactants. Nat. Geosci. 2018, 11, 492–496. [Google Scholar] [CrossRef]
  66. Romano, J.C. Sea-surface slick occurrence in the open sea (Mediterranean, Red Sea, Indian Ocean) in relation to wind speed. Deep Sea Res. Part I Oceanogr. Res. Pap. 1996, 43, 411–423. [Google Scholar] [CrossRef]
  67. Sieburth, J.M.; Conover, J.T. Slicks associated with Trichodesmium blooms in the Sargasso Sea. Nature 1965, 205, 830. [Google Scholar] [CrossRef]
  68. Wurl, O.; Bird, K.; Cunliffe, M.; Landing, W.M.; Miller, U.; Mustaffa, N.I.H.; Ribas-Ribas, M.; Witte, C.; Zappa, C.J. Warming and inhibition of salinization at the ocean’s surface by cyanobacteria. Geophys. Res. Lett. 2018, 45, 4230–4237. [Google Scholar] [CrossRef] [PubMed]
  69. Maynard, N.G. Aquatic foams as an ecological habitat. Zeitschrift für allgemeine Mikrobiologie 1968, 8, 119–126. [Google Scholar] [CrossRef] [PubMed]
  70. Eisenreich, S.J.; Elzerman, A.W.; Armstrong, D.E. Enrichment of micronutrients, heavy metals, and chlorinated hydrocarbons in wind-generated lake foam. Environ. Sci. Technol. 1978, 12, 413–417. [Google Scholar] [CrossRef]
  71. Napolitano, G.E.; Cicerone, D.S. Lipids in water-surface microlayers and foams. In Lipids in Freshwater Ecosystems; Springer: New York, NY, USA, 1999; pp. 235–262. [Google Scholar]
  72. Thingstad, T.F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 2000, 45, 1320–1328. [Google Scholar] [CrossRef] [Green Version]
  73. Tapper, M.A.; Hicks, R.E. Temperate viruses and lysogeny in lake superior bacterioplankton. Limnol. Oceanogr. 1998, 43, 95–103. [Google Scholar] [CrossRef]
  74. Joux, F.; Agogué, H.; Obernosterer, I.; Dupuy, C.; Reinthaler, T.; Herndl, G.J.; Lebaron, P. Microbial community structure in the sea surface microlayer at two contrasting coastal sites in the northwestern Mediterranean Sea. Aquat. Microb. Ecol. 2006, 42, 91–104. [Google Scholar] [CrossRef] [Green Version]
  75. GESAMP (IMO/FAO/UNESCO-IOC/WMO/WHO/IAEA/UN/UNEP Joint Group of Experts on the Scientific Aspects of Marine Environemental Protection). Biological effects of chemical and radiative change in the sea surface. In The Sea-Surface Microlayer and Its Role in Global Change; WMO: Geneva, Switzerland, 1995; Volume 59, pp. 27–51. [Google Scholar]
  76. Kuznetsova, M.; Lee, C.; Aller, J.; Frew, N. Enrichment of amino acids in the sea surface microlayer at coastal and open ocean sites in the North Atlantic Ocean. Limnol. Oceanogr. 2004, 49, 1605–1619. [Google Scholar] [CrossRef] [Green Version]
  77. Culley, A.I.; Welschmeyer, N.A. The abundance, distribution, and correlation of viruses, phytoplankton, and prokaryotes along a Pacific Ocean transect. Limnol. Oceanogr. 2002, 47, 1508–1513. [Google Scholar] [CrossRef] [Green Version]
  78. Maranger, R.; Bird, D.F. Viral abundance in aquatic systems:A comparison between marine and fresh waters. Mar. Ecol. Progr. Ser. 1995, 121, 217–226. [Google Scholar] [CrossRef]
  79. Rahlff, J.; Stolle, C.; Giebel, H.A.; Ribas-Ribas, M.; Damgaard, L.R.; Wurl, O. Oxygen profiles across the sea-surface microlayer-effects of diffusion and biological activity. Front. Mar. Sci. 2019, 6. [Google Scholar] [CrossRef]
  80. Knowles, B.; Silveira, C.B.; Bailey, B.A.; Barott, K.; Cantu, V.A.; Cobian-Guemes, A.G.; Coutinho, F.H.; Dinsdale, E.A.; Felts, B.; Furby, K.A.; et al. Lytic to temperate switching of viral communities. Nature 2016, 531, 466–470. [Google Scholar] [CrossRef] [PubMed]
  81. Ram, A.S.P.; Mari, X.; Brune, J.; Torreton, J.P.; Chu, V.T.; Raimbault, P.; Niggemann, J.; Sime-Ngando, T. Bacterial-viral interactions in the sea surface microlayer of a black carbon-dominated tropical coastal ecosystem (Halong Bay, Vietnam). Elementa-Sci. Anthrop. 2018, 6, 13. [Google Scholar] [Green Version]
  82. Sullivan, M.B.; Waterbury, J.B.; Chisholm, S.W. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 2003, 424, 1047–1051. [Google Scholar] [CrossRef]
  83. Kuznetsova, M.; Lee, C.; Aller, J. Characterization of the proteinaceous matter in marine aerosols. Mar. Chem. 2005, 96, 359–377. [Google Scholar] [CrossRef]
  84. Aller, J.Y.; Kuznetsova, M.R.; Jahns, C.J.; Kemp, P.F. The sea surface microlayer as a source of viral and bacterial enrichment in marine aerosols. J. Aerosol Sci. 2005, 36, 801–812. [Google Scholar] [CrossRef]
  85. Woodcock, A.H. Subsurface pelagic Sargassum. J. Mar. Res. 1950, 9, 77–92. [Google Scholar]
  86. Castello, J.D. Detection of infectious tomato mosaic tobamovirus in fog and clouds. Phytopathology 1995, 85, 1409–1412. [Google Scholar] [CrossRef]
  87. Rastelli, E.; Corinaldesi, C.; Dell’Anno, A.; Lo Martire, M.; Greco, S.; Cristina Facchini, M.; Rinaldi, M.; O’Dowd, C.; Ceburnis, D.; Danovaro, R. Transfer of labile organic matter and microbes from the ocean surface to the marine aerosol: An experimental approach. Sci. Rep. 2017, 7, 11475. [Google Scholar] [CrossRef] [PubMed]
  88. Sharoni, S.; Trainic, M.; Schatz, D.; Lehahn, Y.; Flores, M.J.; Bidle, K.D.; Ben-Dor, S.; Rudich, Y.; Koren, I.; Vardi, A. Infection of phytoplankton by aerosolized marine viruses. Proc. Natl. Acad. Sci. USA 2015, 112, 6643–6647. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Reche, I.; D’Orta, G.; Mladenov, N.; Winget, D.M.; Suttle, C.A. Deposition rates of viruses and bacteria above the atmospheric boundary layer. ISME J. 2018, 12, 1154–1162. [Google Scholar] [CrossRef] [PubMed]
  90. Short, C.M.; Suttle, C.A. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl. Environ. Microbiol. 2005, 71, 480–486. [Google Scholar] [CrossRef] [PubMed]
  91. Breitbart, M.; Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 2005, 13, 278–284. [Google Scholar] [CrossRef] [PubMed]
  92. Mojib, N.; Thimma, M.; Kumaran, M.; Sougrat, R.; Irigoien, X. Comparative metatranscriptomics reveals decline of a neustonic planktonic population. Limnol. Oceanogr. 2017, 62, 299–310. [Google Scholar] [CrossRef]
  93. Zaitsev, Y.P. Marine Neustonology; National Technical Information Service: Springfield, VA, USA, 1971. [Google Scholar]
  94. Frada, M.J.; Schatz, D.; Farstey, V.; Ossolinski, J.E.; Sabanay, H.; Ben-Dor, S.; Koren, I.; Vardi, A. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr. Biol. 2014, 24, 2592–2597. [Google Scholar] [CrossRef] [PubMed]
  95. Wilhelm, S.W.; Weinbauer, M.G.; Suttle, C.A.; Pledger, R.J.; Mitchell, D.L. Measurements of DNA damage and photoreactivation imply that most viruses in marine surface waters are infective. Aquat. Microb. Ecol. 1998, 14, 215–222. [Google Scholar] [CrossRef] [Green Version]
  96. Jiang, S.C.; Paul, J.H. Significance of lysogeny in the marine environment: Studies with isolates and a model of lysogenic phage production. Microb. Ecol. 1998, 35, 235–243. [Google Scholar] [CrossRef] [PubMed]
  97. Wilcox, R.M.; Fuhrman, J.A. Bacterial-viruses in coastal seawater—Lytic rather than lysogenic production. Mar. Ecol. Prog. Ser. 1994, 114, 35–45. [Google Scholar] [CrossRef]
  98. Jiang, S.C.; Paul, J.H. Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar. Ecol. Progr. Ser. 1996, 142, 27–38. [Google Scholar] [CrossRef] [Green Version]
  99. Guitart, C.; Garcia-Flor, N.; Bayona, J.M.; Albaiges, J. Occurrence and fate of polycyclic aromatic hydrocarbons in the coastal surface microlayer. Mar. Pollut. Bull. 2007, 54, 186–194. [Google Scholar] [CrossRef] [PubMed]
  100. Payet, J.P.; Suttle, C.A. To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status. Limnol. Oceanogr. 2013, 58, 465–474. [Google Scholar] [CrossRef] [Green Version]
  101. Roux, S.; Enault, F.; Hurwitz, B.L.; Sullivan, M.B. VirSorter: Mining viral signal from microbial genomic data. PeerJ 2015, 3, e985. [Google Scholar] [CrossRef] [PubMed]
  102. Ren, J.; Ahlgren, N.A.; Lu, Y.Y.; Fuhrman, J.A.; Sun, F. VirFinder: A novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 2017, 5, 69. [Google Scholar] [CrossRef] [PubMed]
  103. Ahlgren, N.A.; Ren, J.; Lu, Y.Y.; Fuhrman, J.A.; Sun, F. Alignment-free d 2 * oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences. Nucleic Acids Res. 2017, 45, 39–53. [Google Scholar] [CrossRef]
  104. Hurwitz, B.L.; Ponsero, A.; Thornton, J.; U’Ren, J.M. Phage hunters: Computational strategies for finding phages in large-scale ’omics datasets. Virus Res. 2018, 244, 110–115. [Google Scholar] [CrossRef]
  105. Andersson, A.F.; Banfield, J.F. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 2008, 320, 1047–1050. [Google Scholar] [CrossRef]
Viruses 11 00191 g001 550
Figure 1. Viral–bacterial dynamics in the surface microlayer (SML) and beyond. DOM = dissolved organic matter, UV = ultraviolet.
Figure 1. Viral–bacterial dynamics in the surface microlayer (SML) and beyond. DOM = dissolved organic matter, UV = ultraviolet.
Viruses 11 00191 g001

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Rahlff, J. The Virioneuston: A Review on Viral–Bacterial Associations at Air–Water Interfaces. Viruses 2019, 11, 191. https://doi.org/10.3390/v11020191

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Rahlff J. The Virioneuston: A Review on Viral–Bacterial Associations at Air–Water Interfaces. Viruses. 2019; 11(2):191. https://doi.org/10.3390/v11020191

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Rahlff, Janina. 2019. "The Virioneuston: A Review on Viral–Bacterial Associations at Air–Water Interfaces" Viruses 11, no. 2: 191. https://doi.org/10.3390/v11020191

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Rahlff, J. (2019). The Virioneuston: A Review on Viral–Bacterial Associations at Air–Water Interfaces. Viruses, 11(2), 191. https://doi.org/10.3390/v11020191

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