Viral Loop Dynamics in Temperate and Polar Freshwaters

All cellular organisms in aquatic environments are susceptible to virus attack. Viruses are the smallest but most abundant biological entities in freshwaters. This thesis describes interactions between viruses and bacteria in temperate and polar freshwaters with particular emphasis on Arctic and Antarctic aquatic systems. Free virus-like particles in freshwaters are vulnerable and exposed and as parasites their survival is dependent on the existence of a suitable host. I found that high concentrations of humic substances in lakes had a negative impact on viral abundance as viruses may be adsorbed to humic matter and replication or viral infectivity may be lost. This indicates that virus-bacteria interactions in humic lakes may differ from those in clear water lakes. Furthermore, there was a high incidence of lysogenic bacteria in humic lakes when compared to other temperate freshwaters which could indicate that lysogeny may act as a viral survival strategy in environments where high rates of destruction and inactivation may occur. On the contrary, I found that lysogenic bacteria were not common in the Arctic and Antarctic freshwaters and during a seasonal study conducted on two Antarctic ultra-oligotrophic lakes lysogenic bacteria were only detected on 3 out of 10 sampling occasions. As viruses are parasites the metabolic state of their host will largely determine how successful they are in replicating. I found that bacterial growth in the Arctic and Antarctic freshwaters was primarily limited by phosphorus however even though an increase in phosphorus had a positive effect on bacteria this was not reflected in the virus abundance. Using electron microscopy I established that a high percentage of the Arctic and Antarctic bacteria population was visibly infected and that the average number of virus-like particles per cell was low relative to previous reported data. This indicates that virus-bacteria interactions in polar freshwaters differ significantly from those in temperate freshwaters. In microbially dominated Antarctic freshwater lakes the major pathway of energy and carbon flow is through the microbial loop. Viral lysis disrupts this flow and shunts organic carbon back into the dissolved organic carbon (DOC) pool making it available for the uninfected bacterial community. I found that viral lysis of bacterial cells could contribute significantly to the DOC pool in Antarctic freshwater lakes. I estimated that over 60% of the carbon supplied to the DOC pool originated from viral lysis during the winter months while during the summer period less than 20% originated from viral lysis. This implies that viral processes in extreme Antarctic lakes may be of quantitative significance with respect to carbon flow

Kelp-associated microbes facilitate spatial subsidy in a detrital-based food web in a shoreline ecosystem

Microbes are ubiquitous but our knowledge of their effects on consumers is limited in benthic marine systems. Shorelines often form hotspots of microbial and detritivore activity due to the large amounts of detrital macrophytes that are exported from other coastal ecosystems, such as kelp forests, and accumulate in these systems. Shoreline ecosystems therefore provide a useful model system to examine microbial-detritivore interactions. We experimentally test whether bacteria in the biofilm of kelp provide a bottom-up influence on growth and reproductive output of detritivores in shorelines where detrital kelp accumulates, by manipulating the bacterial abundances on kelp (Ecklonia radiata). The growth rates for both male and female amphipods (Allorchestes compressa) were greater in treatments containing bacteria than those in which bacteria were reduced through antibiotic treatment, and this effect was greater for males offered aged kelp. The proportions of ovigerous females were greater when reared on kelp with intact bacteria, indicating a more rapid reproductive development in the presence of more bacteria. Bacterial abundance had little to no influence on nutrient content and palatability of kelp, based on tissue toughness, nitrogen and carbon content and C:N ratio. Thus, the most likely pathway for a microbial effect on detritivores was through feeding on kelp-associated bacteria. Regardless of the pathway, kelp-associated microbes have a strong influence on the fitness of a highly abundant detritivore that feeds preferentially on E. radiata in shoreline systems, and therefore form a hidden trophic step in this “brown” food web and a hotspot of secondary production

Coastal connectivity and spatial subsidy from a microbial perspective

© 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. The transfer of organic material from one coastal environment to another can increase production in recipient habitats in a process known as spatial subsidy. Microorganisms drive the generation, transformation, and uptake of organic material in shallow coastal environments, but their significance in connecting coastal habitats through spatial subsidies has received limited attention. We address this by presenting a conceptual model of coastal connectivity that focuses on the flow of microbially mediated organic material in key coastal habitats. Our model suggests that it is not the difference in generation rates of organic material between coastal habitats but the amount of organic material assimilated into microbial biomass and respiration that determines the amount of material that can be exported from one coastal environment to another. Further, the flow of organic material across coastal habitats is sensitive to environmental change as this can alter microbial remineralization and respiration rates. Our model highlights microorganisms as an integral part of coastal connectivity and emphasizes the importance of including a microbial perspective in coastal connectivity studies

The role of glacier mice in the invertebrate colonisation of glacial surfaces: the moss balls of the Falljökull, Iceland

Glacier surfaces have a surprisingly complex ecology. Cryoconite holes contain diverse invertebrate communities while other invertebrates, such as Collembola often graze on algae and windblown dead organic on the glacier surface. Glacier mice (ovoid unattached moss balls) occur on some glaciers worldwide. Studies of these glacier mice have concentrated on their occurrence and mode of formation. There are no reports of the invertebrate communities. But, such glacier mice may provide a suitable favourable habitat and refuge for a variety of invertebrate groups to colonise the glacier surface. Here we describe the invertebrate fauna of the glacier mice (moss balls) of the Falljökull, Iceland. The glacier mice were composed of Racomitrium sp. and varied in size from 8.0 to 10.0 cm in length. All glacier mice studied contained invertebrates. Two species of Collembola were present. Pseudisotoma sensibilis (Tullberg, 1876) was numerically dominant with between 12 and 73 individuals per glacier mouse while Desoria olivacea (Tullberg, 1871) occurred but in far lower numbers. Tardigrada and Nematoda had mean densities of approximately 200 and 1,000 respectively. No Acari, Arachnida or Enchytraeidae were observed which may be related to the difficulty these groups have in colonizing the glacier mice. We suggest that glacier mice provide an unusual environmentally ameliorated microhabitat for an invertebrate community dwelling on a glacial surface. The glacier mice thereby enable an invertebrate fauna to colonise an otherwise largely inhospitable location with implications for carbon flow in the system

Nitrate addition has minimal short-term impacts on Greenland ice sheet supraglacial prokaryotes

Tropospheric nitrate levels are predicted to increase throughout the 21st century, with potential effects on terrestrial ecosystems, including the Greenland ice sheet (GrIS). This study considers the impacts of elevated nitrate concentrations on the abundance and composition of dominant bulk and active prokaryotic communities sampled from in situ nitrate fertilization plots on the GrIS surface. Nitrate concentrations were successfully elevated within sediment-filled meltwater pools, known as cryoconite holes; however, nitrate additions applied to surface ice did not persist. Estimated bulk and active cryoconite community cell abundance was unaltered by nitrate additions when compared to control holes using a quantitative PCR approach, and nitrate was found to have a minimal affect on the dominant 16S rRNA gene-based community composition. Together, these results indicate that sampled cryoconite communities were not nitrate limited at the time of sampling. Instead, temporal changes in biomass and community composition were more pronounced. As these in situ incubations were short (6 weeks), and the community composition across GrIS surface ice is highly variable, we suggest that further efforts should be considered to investigate the potential long-term impacts of increased nitrate across the GrIS

Variations of algal communities cause darkening of a Greenland glacier

We have assessed the microbial ecology on the surface of Mittivakkat glacier in SE-Greenland during the exceptional high melting season in July 2012 when the so far most extreme melting rate for the Greenland Ice Sheet has been recorded. By employing a complementary and multi-disciplinary field sampling and analytical approach, we quantified the dramatic changes in the different microbial surface habitats (green snow, red snow, biofilms, grey ice, cryoconite holes). The observed clear change in dominant algal community and their rapidly changing cryo-organic adaptation inventory was linked to the high melting rate. The changes in carbon and nutrient fluxes between different microbial pools (from snow to ice, cryoconite holes and glacial forefronts) revealed that snow and ice algae dominate the net primary production at the onset of melting, and that they have the potential to support the cryoconite hole communities as carbon and nutrient sources. A large proportion of algal cells is retained on the glacial surface and temporal and spatial changes in pigmentation contribute to the darkening of the snow and ice surfaces. This implies that the fast, melt-induced algal growth has a high albedo reduction potential, and this may lead to a positive feedback speeding up melting processes

Maximum in the Middle: Nonlinear Response of Microbial Plankton to Ultraviolet Radiation and Phosphorus

The responses of heterotrophic microbial food webs (HMFW) to the joint action of abiotic stressors related to global change have been studied in an oligotrophic high-mountain lake. A 2×5 factorial design field experiment performed with large mesocosms for >2 months was used to quantify the dynamics of the entire HMFW (bacteria, heterotrophic nanoflagellates, ciliates, and viruses) after an experimental P-enrichment gradient which approximated or surpassed current atmospheric P pulses in the presence vs. absence of ultraviolet radiation. HMFW underwent a mid-term (<20 days) acute development following a noticeable unimodal response to P enrichment, which peaked at intermediate P-enrichment levels and, unexpectedly, was more accentuated under ultraviolet radiation. However, after depletion of dissolved inorganic P, the HMFW collapsed and was outcompeted by a low-diversity autotrophic compartment, which constrained the development of HMFW and caused a significant loss of functional biodiversity. The dynamics and relationships among variables, and the response patterns found, suggest the importance of biotic interactions (predation/parasitism and competition) in restricting HMFW development, in contrast to the role of abiotic factors as main drivers of autotrophic compartment. The response of HMFW may contribute to ecosystem resilience by favoring the maintenance of the peculiar paths of energy and nutrient-mobilization in these pristine ecosystems, which are vulnerable to threats by the joint action of abiotic stressors related to global change.This research was supported by Junta de Andalucía (Excelencia P07-CVI-02598 to PC, and P09-RNM-5376 to JMMS), the Spanish Ministries of Medio Ambiente, Rural y Marino (PN2009/067 to PC) and Ciencia e Innovación (GLC2008-01127/BOS and CGL2011-23681 to PC), the ERC Advanced Grant project number 250254 “MINOS” (to GB), and two Spanish government grants (to JADM and FJB)

Effect of temperature on rates of ammonium uptake and nitrification in the western coastal Arctic during winter, spring, and summer

Biogeochemical rate processes in the Arctic are not currently well constrained, and there is very limited information on how rates may change as the region warms. Here we present data on the sensitivity of ammonium (NH4+) uptake and nitrification rates to short-term warming. Samples were collected from the Chukchi Sea off the coast of Barrow, Alaska, during winter, spring, and summer and incubated for 24h in the dark with additions of (NH4+)-N-15 at -1.5, 6, 13, and 20 degrees C. Rates of NH4+ uptake and nitrification were measured in conjunction with bacterial production. In all seasons, NH4+ uptake rates were highest at temperatures similar to current summertime conditions but dropped off with increased warming, indicative of psychrophilic (i.e., cold-loving) microbial communities. In contrast, nitrification rates were less sensitive to temperature and were higher in winter and spring compared to summer. These findings suggest that as the Arctic coastal ecosystem continues to warm, NH4+ assimilation may become increasingly important, relative to nitrification, although the magnitude of NH4+ assimilation would be still be lower than nitrification

Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard

The diversity of highly active bacterial communities in cryoconite holes on three Arctic glaciers in Svalbard was investigated using terminal restriction fragment length polymorphism (T-RFLP) of the 16S rRNA locus. Construction and sequencing of clone libraries allowed several members of these communities to be identified, with Proteobacteria being the dominant one, followed by Cyanobacteria and Bacteroidetes. T-RFLP data revealed significantly different communities in holes on the (cold) valley glacier Austre Brøggerbreen relative to two adjacent (polythermal) valley glaciers, Midtre Lovénbreen and Vestre Brøggerbreen. These population compositions correlate with differences in organic matter content, temperature and the metabolic activity of microbial communities concerned. No within-glacier spatial patterns were observed in the communities identified over the 2-year period and with the 1 km-spaced sampling. We infer that surface hydrology is an important factor in the development of cryoconite bacterial communities