Sanni L. Aalto

A three-way perspective of stoichiometric changes on host-parasite interactions

Changes in environmental nutrients play a crucial role in driving disease dynamics, but global patterns in nutrient-driven changes in disease are difficult to predict. In this paper we use ecological stoichiometry as a framework to review host-parasite interactions under changing nutrient ratios, focusing on three pathways: (i) altered host resistance and parasite virulence through host stoichiometry (ii) changed encounter or contact rates at population level, and (iii) changed host community structure. We predict that the outcome of nutrient changes on host-parasite interactions depends on which pathways are modified, and suggest that the outcome of infection could depend on the overlap in stoichiometric requirements of the host and the parasite. We hypothesize that environmental nutrient enrichment alters infectivity dynamics leading to fluctuating selection dynamics in host-parasite coevolution.

Terrestrial carbohydrates support freshwater zooplankton during phytoplankton deficiency

Freshwater food webs can be partly supported by terrestrial primary production, often deriving from plant litter of surrounding catchment vegetation. Although consisting mainly of poorly bioavailable lignin, with low protein and lipid content, the carbohydrates from fallen tree leaves and shoreline vegetation may be utilized by aquatic consumers. Here we show that during phytoplankton deficiency, zooplankton (Daphnia magna) can benefit from terrestrial particulate organic matter by using terrestrial-origin carbohydrates for energy and sparing essential fatty acids and amino acids for somatic growth and reproduction. Assimilated terrestrial-origin fatty acids from shoreline reed particles exceeded available diet, indicating that Daphnia may convert a part of their dietary carbohydrates to saturated fatty acids. This conversion was not observed with birch leaf diets, which had lower carbohydrate content. Subsequent analysis of 21 boreal and subarctic lakes showed that diet of herbivorous zooplankton is mainly based on high-quality phytoplankton rich in essential polyunsaturated fatty acids. The proportion of low-quality diets (bacteria and terrestrial particulate organic matter) was <28% of the assimilated carbon. Taken collectively, the incorporation of terrestrial carbon into zooplankton was not directly related to the concentration of terrestrial organic matter in experiments or lakes, but rather to the low availability of phytoplankton.

Food stoichiometry affects the outcome of Daphnia–parasite interaction

Phosphorus (P) is an essential nutrient for growth in consumers. P-limitation and parasite infection comprise one of the most common stressor pairs consumers confront in nature. We conducted a life-table study using a Daphnia–microsporidian parasite model, feeding uninfected or infected Daphnia with either P-sufficient or P-limited algae, and assessed the impact of the two stressors on life-history traits of the host. Both infection and P-limitation negatively affected some life-history traits tested. However, under P-limitation, infected animals had higher juvenile growth rate as compared with uninfected animals. All P-limited individuals died before maturation, regardless of infection. The numbers of spore clusters of the microsporidian parasite did not differ in P-limited or P-sufficient hosts. P-limitation, but not infection, decreased body phosphorus content and ingestion rates of Daphnia tested in separate experiments. As parasite spore production did not suffer even under extreme P-limitation, our results suggest that parasite was less limited by P than the host. We discuss possible interpretations concerning the stoichiometrical demands of parasite and suggest that our results are explained by parasite-driven changes in carbon (C) allocation of the hosts. We conclude that the impact of nutrient starvation and parasite infection on consumers depends not only on the stoichiometric demands of host but also those of the parasite.

Microbial Community Response on Wastewater Discharge in Boreal Lake Sediments

Despite high performance, municipal wastewater treatment plants (WWTPs) still discharge significant amounts of organic material and nitrogen and even microbes into the receiving water bodies, altering physico-chemical conditions and microbial functions. In this study, we examined how nitrified wastewater affects the microbiology of boreal lake sediments. Microbial community compositions were assessed with next generation sequencing of the 16S rRNA gene, and a more detailed view on nitrogen transformation processes was gained with qPCR targeting on functional genes (nirS, nirK, nosZI, nosZII, amoAarchaea, and amoAbacteria). In both of the two studied lake sites, the microbial community composition differed significantly between control point and wastewater discharge point, and a gradual shift toward natural community composition was seen downstream following the wastewater gradient. SourceTracker analysis predicted that ∼2% of sediment microbes were of WWTP-origin on the study site where wastewater was freely mixed with the lake water, while when wastewater was specially discharged to the sediment surface, ∼6% of microbes originated from WWTP, but the wastewater-influenced area was more limited. In nitrogen transformation processes, the ratio between nitrifying archaea (AOA) and bacteria (AOB) was affected by wastewater effluent, as the AOA abundance decreased from the control point (AOA:AOB 28:1 in Keuruu, 11:1 in Petäjävesi) to the wastewater-influenced sampling points, where AOB dominated (AOA:AOB 1:2–1:15 in Keuruu, 1:3–1:19 in Petäjävesi). The study showed that wastewater can affect sediment microbial community through importing nutrients and organic material and altering habitat characteristics, but also through bringing wastewater-originated microbes to the sediment, and may thus have significant impact on the freshwater biogeochemistry, especially in the nutrient-poor boreal ecosystems.

Bacterial community response to changes in a tri‐trophic cascade during a whole‐lake fish manipulation

Microbial communities play a key role in biogeochemical processes by degrading organic material and recycling nutrients, but can also be important food sources for upper trophic levels. Trophic cascades might modify microbial communities either directly via grazing or indirectly by inducing changes.in other biotic or in abiotic factors (e.g., nutrients). We studied the effects of a tri-trophic cascade on microbial communities during a whole-lake manipulation in which European perch (Perca fluviatilis) were added to a naturally fishless lake divided experimentally into two basins. We measured environmental parameters (oxygen, temperature, and nutrients) and zooplankton biomass and studied the changes in the bacterial community using next generation sequencing of 16S rRNA genes and cell counting. Introduction of fish reduced the biomass of zooplankton, mainly Daphnia, which partly altered the bacterial community composition and affected the bacterial cell abundances. However, the microbial community composition was mainly governed by stratification patterns and associated vertical oxygen concentration. Slowly growing green sulfur bacteria (Chlorobium) dominated the anoxic water layers together with bacteria of the candidate division ODI. We conclude that alterations in trophic interactions can affect microbial abundance, but that abiotic factors seem to be more significant controls of microbial community composition in sheltered boreal lakes.

No uniform associations between parasite prevalence and environmental nutrients

The resource quality of the host has been shown to affect parasite transmission success, prevalence, and virulence. Seasonal availability of environmental nutrients alters density and stoichiometric quality (carbon–nutrient ratios) of both producers and consumers, suggesting that nutrient availability may drive fluctuations in parasite prevalence patterns observed in nature. We examined the interactions between the population dynamics of a keystone herbivore, Daphnia, and its parasites, and their associations with water nutrient concentrations, resource quantity and quality, and other environmental variables (temperature, pH, oxygen concentration) in a small lake, using general linear models. We found that the prevalence of two gut endoparasites was positively related to food source and quality as well as nitrogen content of Daphnia, whereas the prevalence of an epibiont and overall parasite species richness was negatively related to phosphorus content of Daphnia. When only endoparasite species richness w...

Responses of algae, bacteria, Daphnia and natural parasite fauna of Daphnia to nutrient enrichment in mesocosms

Understanding responses of parasites to changes in nutrient regimes is necessary for prediction of their role in aquatic ecosystems under global change in nutrient loading. We studied the response of the natural parasite fauna of Daphnia longispina to nutrient enrichment in mesocosms in a small humic lake. We measured the concentrations of inorganic phosphorus and nitrogen in the water, total nutrients in the seston, algal and bacterial biomass, Daphnia population dynamics, Daphnia stoichiometry, Daphnia stable isotope values and the presence and abundance of parasites in treated mesocosms as compared to three control ones. Incorporation of the nutrient enrichment in the food web was seen as increased nutrient concentrations in the epilimnion and as a decrease in carbon:nutrient ratios and δ15N values in Daphnia. Nutrient enrichment did not significantly influence algal, bacterial or Daphnia biomass. One of the four parasite species observed, unidentified small gut parasite, had a higher prevalence (percentage of Daphnia infected) in treated mesocosms, but its intensity (number of parasites per infected host) remained the same among treatments. Our results suggest that the effect of nutrient enrichment on host–parasite dynamics is dependent on complex interactions within food webs and on the epidemiological traits of parasites.

The Importance of Phytoplankton Biomolecule Availability for Secondary Production

The growth and reproduction of animals is affected by their access to resources. In aquatic ecosystems, the availability of essential biomolecules for filter-feeding zooplankton dependents greatly on phytoplankton. Here, we analyzed the biochemical composition, i.e., the fatty acid, sterol and amino acid profiles and concentrations as well as protein, carbon, nitrogen and phosphorus content of 17 phytoplankton monocultures representing the seven most abundant phytoplankton classes in boreal and sub-arctic lakes. To examine how the differences in the biochemical composition between phytoplankton classes affect their nutritional quality for consumers, we assessed the performance of Daphnia, on these diets. Furthermore, we defined the most important biomolecules regulating the somatic growth and reproduction of Daphnia, expecting that higher concentrations of certain biomolecules are needed for reproduction than for growth. Finally, we combined these results with phytoplankton field data from over 900 boreal and sub-arctic lakes in order to estimate whether the somatic growth of Daphnia is sterol-limited when the natural phytoplankton communities are cyanobacteria-dominated. Our analysis shows that Daphnia grows best with phytoplankton rich in sterols, ω-3 fatty acids, protein and amino acids. Their reproduction follows food sterol and ω-3 concentration as well as C:P-ratio being two times higher in Daphnia feeding on cryptophytes than any other diet. Interestingly, we found that a high dietary ω-6 fatty acid concentration decreases both somatic growth and reproduction of Daphnia. When combined with phytoplankton community composition field data, our results indicate that zooplankton is constantly limited by sterols in lakes dominated by cyanobacteria (≥ 40 % of total phytoplankton biomass), and that the absence of cryptophytes can severely hinder zooplankton production in nature.

Sediment diffusion method improves wastewater nitrogen removal in the receiving lake sediments

Sediment microbes have a great potential to transform reactive N to harmless N2, thus decreasing wastewater nitrogen load into aquatic ecosystems. Here, we examined if spatial allocation of the wastewater discharge by a specially constructed sediment diffuser pipe system enhanced the microbial nitrate reduction processes. Full-scale experiments were set on two Finnish lake sites, Keuruu and Petäjävesi, and effects on the nitrate removal processes were studied using the stable isotope pairing technique. All nitrate reduction rates followed nitrate concentrations, being highest at the wastewater-influenced sampling points. Complete denitrification with N2 as an end-product was the main nitrate reduction process, indicating that the high nitrate and organic matter concentrations of wastewater did not promote nitrous oxide (N2O) production (truncated denitrification) or ammonification (dissimilatory nitrate reduction to ammonium; DNRA). Using 3D simulation, we demonstrated that the sediment diffusion method enhanced the contact time and amount of wastewater near the sediment surface especially in spring and in autumn, altering organic matter concentration and oxygen levels, and increasing the denitrification capacity of the sediment. We estimated that natural denitrification potentially removed 3-10% of discharged wastewater nitrate in the 33 ha study area of Keuruu, and the sediment diffusion method increased this areal denitrification capacity on average 45%. Overall, our results indicate that sediment diffusion method can supplement wastewater treatment plant (WWTP) nitrate removal without enhancing alternative harmful processes.

Novel Autotrophic Organisms Contribute Significantly to the Internal Carbon Cycling Potential of a Boreal Lake

ABSTRACT Oxygen-stratified lakes are typical for the boreal zone and also a major source of greenhouse gas emissions in the region. Due to shallow light penetration, restricting the growth of phototrophic organisms, and large allochthonous organic carbon inputs from the catchment area, the lake metabolism is expected to be dominated by heterotrophic organisms. In this study, we test this assumption and show that the potential for autotrophic carbon fixation and internal carbon cycling is high throughout the water column. Further, we show that during the summer stratification carbon fixation can exceed respiration in a boreal lake even below the euphotic zone. Metagenome-assembled genomes and 16S profiling of a vertical transect of the lake revealed multiple organisms in an oxygen-depleted compartment belonging to novel or poorly characterized phyla. Many of these organisms were chemolithotrophic, potentially deriving their energy from reactions related to sulfur, iron, and nitrogen transformations. The community, as well as the functions, was stratified along the redox gradient. The autotrophic potential in the lake metagenome below the oxygenic zone was high, pointing toward a need for revising our concepts of internal carbon cycling in boreal lakes. Further, the importance of chemolithoautotrophy for the internal carbon cycling suggests that many predicted climate change-associated fluctuations in the physical properties of the lake, such as altered mixing patterns, likely have consequences for the whole-lake metabolism even beyond the impact to the phototrophic community. IMPORTANCE Autotrophic organisms at the base of the food web are the only life form capable of turning inorganic carbon into the organic form, facilitating the survival of all other organisms. In certain environments, the autotrophic production is limited by environmental conditions and the food web is supported by external carbon inputs. One such environment is stratified boreal lakes, which are one of the biggest natural sources of greenhouse gas emissions in the boreal region. Thus, carbon cycling in these habitats is of utmost importance for the future climate. Here, we demonstrate a high potential for internal carbon cycling via phototrophic and novel chemolithotrophic organisms in the anoxic, poorly illuminated layers of a boreal lake. Our results significantly increase our knowledge on the microbial communities and their metabolic potential in oxygen-depleted freshwaters and help to understand and predict how climate change-induced alterations could impact the lake carbon dynamics. IMPORTANCE Autotrophic organisms at the base of the food web are the only life form capable of turning inorganic carbon into the organic form, facilitating the survival of all other organisms. In certain environments, the autotrophic production is limited by environmental conditions and the food web is supported by external carbon inputs. One such environment is stratified boreal lakes, which are one of the biggest natural sources of greenhouse gas emissions in the boreal region. Thus, carbon cycling in these habitats is of utmost importance for the future climate. Here, we demonstrate a high potential for internal carbon cycling via phototrophic and novel chemolithotrophic organisms in the anoxic, poorly illuminated layers of a boreal lake. Our results significantly increase our knowledge on the microbial communities and their metabolic potential in oxygen-depleted freshwaters and help to understand and predict how climate change-induced alterations could impact the lake carbon dynamics.