Contrasting Mixotrophic Lifestyles Reveal Different Ecological Niches in Two Closely Related Marine Protists

Many marine microbial eukaryotes combine photosynthetic with phagotrophic nutrition, but incomplete understanding of such mixotrophic protists, their functional diversity, and underlying physiological mechanisms limits the assessment and modeling of their roles in present and future ocean ecosystems. We developed an experimental system to study responses of mixotrophic protists to availability of living prey and light, and used it to characterize contrasting physiological strategies in two stramenopiles in the genus Ochromonas. We show that oceanic isolate CCMP1393 is an obligate mixotroph, requiring both light and prey as complementary resources. Interdependence of photosynthesis and heterotrophy in CCMP1393 comprises a significant role of mitochondrial respiration in photosynthetic electron transport. In contrast, coastal isolate CCMP2951 is a facultative mixotroph that can substitute photosynthesis by phagotrophy and hence grow purely heterotrophically in darkness. In contrast to CCMP1393, CCMP2951 also exhibits a marked photoprotection response that integrates non-photochemical quenching and mitochondrial respiration as electron sink for photosynthetically produced reducing equivalents. Facultative mixotrophs similar to CCMP2951 might be well adapted to variable environments, while obligate mixotrophs similar to CCMP1393 appear capable of resource efficient growth in oligotrophic ocean environments. Thus, the responses of these phylogenetically close protists to the availability of different resources reveals niche differentiation that influences impacts in food webs and leads to opposing carbon cycle roles.     

Diversity and Distributional Patterns of Ciliates in Guaymas Basin Hydrothermal Vent Sediments

Little is known about protists at deep‐sea hydrothermal vents. The vent sites at Guaymas Basin in the Gulf of California are characterized by dense mats of filamentous pigmented or nonpigmented Beggiatoa that serve as markers of subsurface thermochemical gradients. We constructed 18S rRNA libraries to investigate ciliate assemblages in Beggiatoa mats and from bare sediments at the Guaymas vent site. Results indicated a high diversity of ciliates, with 156 operational taxonomic units identified in 548 sequences. Comparison between mat environments demonstrated that ciliate and bacterial assemblages from pigmented mats, nonpigmented mats, and bare sediments were significantly different and highly correlated with bacterial assemblages. Neither bacterial nor ciliate assemblages were correlated with environmental factors. The most abundant ciliates at Guaymas were more likely to be represented in clone libraries from other hydrothermal, deep‐sea, and/or anoxic or microaerophilic environments, supporting the hypothesis that these ciliate species are broadly distributed. The orange mat environment included a higher proportion of ciliate sequences that were more similar to those from other environmental studies than to cultured ciliate species, whereas clone libraries from bare sediments included sequences that were the most highly divergent from all other sequences and may represent species that are endemic to Guaymas.     

Towards a Molecular Taxonomy for Protists: Benefits,Risks, and Applications in Plankton Ecology

The increasing use of genetic information for the development of methods to study the diversity, distributions, and activities of protists in nature has spawned a new generation of powerful tools. For ecologists, one lure of these approaches lies in the potential for DNA sequences to provide the only immediately obvious means of normalizing the diverse criteria that presently exist for identifying and counting protists. A single, molecular taxonomy would allow studies of diversity across a broad range of species, as well as the detection and quantification of particular species of interest within complex, natural assemblages; goals that are not feasible using traditional methods. However, these advantages are not without their potential pitfalls and problems. Conflicts involving the species concept, disagreements over the true (physiological/ecological) meaning of genetic diversity, and a perceived threat by some that sequence information will displace knowledge regarding the morphologies, functions and physiologies of protistan taxa, have created debate and doubt regarding the efficacy and appropriateness of some genetic approaches. These concerns need continued discussion and eventual resolution as we move toward the irresistible attraction, and potentially enormous benefits, of the application of genetic approaches to protistan ecology.     

Ecology of Some Ricefields in Japan as Exemplified by Some Benthic Fauna,with Notes on Management

The role of tubificids and mud snails in the ricefield ecosystem was elucidated using their ecology as a basis for highlighting problems in the strategy of recycling between agricultural and urban activities. Tubificid oligochaetes occur in high densities in ricefields where irrigation water is polluted with sewage, high organic matter content is present in the soil and when highly toxic insecticides are not used. High tubificid densities reduce and even eliminate weeds, change the composition and density of bacteria and increase the density of zooplankton. Also they serve as a high quality source of food for fish comparable to that of insects. Conditions that promote a healthy growth of tubificids obviate or reduce the need for weedicides and high levels of inorganic fertilizers. Mud snails which thrive in ricefields have been used as an important source of protein food for humans in rural Japan. The snails can consume a sludge-reed compost mixture used as a fertilizer in ricefields. However the high heavy metal content in the sludge is accumulated by the snails which are thus unfit for human consumption. Based on these results and the known ecology of tubificids and the snails, a possible recycling system comprising sewage sludge, reeds, fish, insects and egrets using these two kinds of benthic organisms is proposed.     

Microbial Communities of Deep Marine Subsurface Sediments: Molecular and Cultivation Surveys

Recent molecular analyses show that microbial communities of deep marine sediments harbor members of distinct, uncultured bacterial and archaeal lineages, in addition to Gram-positive bacteria and Proteobacteria that are detected by cultivation surveys. Several of these subsurface lineages show cosmopolitan occurrence patterns; they can be found in cold marine sediments and also in hydrothermal habitats, suggesting a continuous deep subsurface and hydrothermal biosphere with shared microbiota. The physiologies and activities of these uncultured subsurface lineages remain to be explored by innovative combinations of genomic and biogeochemical approaches.     

Geochemistry and Microbial Populations in Sediments of the Northern Baffin Bay,Arctic

The Northern Baffin Bay between Greenland and Canada is a remote Arctic area restricted in primary production by seasonal ice cover, with presumably low sedimentation rates, carbon content and microbial activities in its sediments. Our aim was to study the so far unknown subseafloor geochemistry and microbial populations driving seafloor ecosystems. Shelf sediments had the highest organic carbon content, numbers of Bacteria and Archaea, and microcosms inoculated from Shelf sediments showed highest sulfate reduction and methane production rates. Sediments in the central deep area and on the southern slope contained less organic carbon and overall lower microbial numbers. Similar 16S rRNA gene copy numbers of Archaea and Bacteria were found for the majority of the sites investigated. Sulfate in pore water correlated with dsrA copy numbers of sulfate-reducing prokaryotes and differed between sites. No methane was found as free gas in the sediments, and mcrA copy numbers of methanogenic Archaea were low. Methanogenic and sulfate-reducing cultures were enriched on a variety of substrates including hydrocarbons. In summary, the Greenlandic shelf sediments contain vital microbial communities adapted to their specific environmental conditions.     

Microbial communities in low permeability,high pH uranium mine tailings: characterization and potential effects

Aims

To describe the diversity and metabolic potential of microbial communities in uranium mine tailings characterized by high pH, high metal concentration and low permeability.

Methods and Results

To assess microbial diversity and their potential to influence the geochemistry of uranium mine tailings using aerobic and anaerobic culture‐based methods, in conjunction with next generation sequencing and clone library sequencing targeting two universal bacterial markers (the 16S rRNA and cpn60 genes). Growth assays revealed that 69% of the 59 distinct culturable isolates evaluated were multiple‐metal resistant, with 15% exhibiting dual‐metal hypertolerance. There was a moderately positive correlation coefficient (R = 0·43, P < 0·05) between multiple‐metal resistance of the isolates and their enzyme expression profile. Of the isolates tested, 17 reduced amorphous iron, 22 reduced molybdate and seven oxidized arsenite. Based on next generation sequencing, tailings depth was shown to influence bacterial community composition, with the difference in the microbial diversity of the upper (0–20 m) and middle (20–40 m) tailings zones being highly significant (P < 0·01) from the lower zone (40–60 m) and the difference in diversity of the upper and middle tailings zone being significant (P < 0·05). Phylotypes closely related to well‐known sulfate‐reducing and iron‐reducing bacteria were identified with low abundance, yet relatively high diversity.

Conclusions

The presence of a population of metabolically‐diverse, metal‐resistant micro‐organisms within the tailings environment, along with their demonstrated capacity for transforming metal elements, suggests that these organisms have the potential to influence the long‐term geochemistry of the tailings.

Significance and Impact of the study

This study is the first investigation of the diversity and functional potential of micro‐organisms present in low permeability, high pH uranium mine tailings.     

Trophic coupling of the microbial and the classical food web in Lake Baikal,Siberia

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Activation of an Aquareovirus,Chum Salmon Reovirus (CSV), by the Ciliates Tetrahymena thermophila and T. canadensis

For the first time, ciliates have been found to activate rather than inactivate a virus, chum salmon reovirus (CSV). Activation was seen as an increase in viral titre upon incubation of CSV at 22 °C with Tetrahymena canadenesis and two strains of T. thermophila: wild type (B1975) and a temperature conditional mutant for phagocytosis (NP1). The titre increase was not likely due to replication because CSV had no visible effects on the ciliates and no vertebrate virus has ever been shown unequivocally to replicate in ciliates. When incubated with B1975 and NP1 at 30 °C, CSV was activated only by B1975. Therefore, activation required CSV internalization because at 30 °C only B1975 exhibited phagocytosis. CSV replicated in fish cells at 18 to 26 °C but not at 30 °C. Collectively, these observations point to CSV activation being distinct from replication. Activation is attributed to the CSV capsid being modified in the ciliate phagosomal‐lysosomal system and released in a more infectious form. When allowed to swim in CSV‐infected fish cell cultures, collected, washed, and transferred to uninfected cultures, T. canadensis caused a CSV infection. Overall the results suggest that ciliates could have roles in the environmental dissemination of some fish viral diseases.     

Benthic community metabolism in four temperate stream systems: An inter-biome comparison and evaluation of the river continuum concept

Benthic community metabolism was studied on four stream systems located in different biomes in the United States: the eastern deciduous forest (Pennsylvania, PA, and Michigan, MI), the high desert (Idaho, ID), and the coniferous forest (Oregon, OR). Studies were designed to test the hypothesis advanced within the River Continuum Concept that a transition in community metabolism will occur from a predominance of heterotrophy in headwaters to a predominance of autotrophy in mid-sized reaches, with a return to heterotrophy further downstream. Both gross primary productivity (GPP) and community respiration (CR₂₄) increased with downstream direction on all systems. Net daily metabolism (NDM, or GPP – CR₂₄) shifted from heterotrophy (–NDM, GPP < CR₂₄) to autotrophy (+NDM, GPP > CR₂₄) with downstream direction at all sites, supporting the hypothesis. Annual metabolism in the most upstream reach of all sites was dominated by respiration; however, the farthest downstream reach was not necessarily the most autotrophic. Site-specific factors affected manifestation of the trend. Photosynthesis predominated annual metabolism in reaches (designated 1–4 in order of increasing size) 2–4 in ID, 3 and 4 in OR, and 4 in MI. In PA annual photosynthesis was slightly greater than respiration only at Station 3. Photosynthesis was predominant most consistently in ID and respiration most often in PA. About half the reaches that were heterotrophic annually were autotrophic at one or more seasons. Annual means of benthic GPP, CR₂₄ and NDM ranged from 0.16 to 3.37, 0.36 to 2.88 and –0.73 to 0.50 g O₂ · m² · d¹, respectively. Metabolic rates were usually high in PA and MI (and sometimes ID) and almost always lowest in OR. Parameters accounting for most variance in multiple linear regression analyses of the combined metabolism data from all sites were indicators of stream size, photosynthetically active radiation, temperature, and chlorophyll a concentration.     

Food webs in space: On the interplay of dynamic instability and spatial processes

Ecologists increasingly recognize that a consideration of spatial dynamics is essential for resolving many classical problems in community ecology. In the present paper, I argue that understanding how trophic interactions influence population stability can have important implications for the expression of spatial processes. I use two examples to illustrate this point. The first example has to do with spatial determinants of food chain length. Prior theoretical and empirical work has suggested that colonization–extinction dynamics can influence food chain length, at least for specialist consumers. I briefly review evidence and prior theory that food chain length is sensitive to area. A metacommunity scenario, in which each of various patches can have a food chain varying in length (but in which a consumer is not present on a patch unless its required resource is also present), shows that alternative landscape states are possible. This possibility arises if top predators moderate unstable interactions between intermediate predators and basal resources. The second example has to do with the impact of recurrent immigration on the stability of persistent populations. Immigration can either stabilize or destabilize local population dynamics. Moreover, an increase in immigration can decrease average population size for unstable populations with direct density-dependence, or in predator–prey systems with saturating functional responses. These theoretical models suggest that the interplay of temporal variation and spatial fluxes can lead to novel qualitative phenomena.     

Seasonal and ontogenetic shifts in the diet of Arctic charr Salvelinus alpinus in a subarctic lake

Seasonal and ontogenetic shifts in the diet of Arctic charr Salvelinus alpinus were studied in a deep, ultra‐oligotrophic lake in subarctic Finland from both stomach contents and the stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope compositions of muscle and liver tissues. Both diet and isotope results indicated that the S. alpinus population relied mainly on littoral benthic energy sources. The strong littoral reliance appeared largely independent of season or fish size, although the data lacked small (total length, L_T, <130 mm) and young (<3 years) S. alpinus. Liver isotope values of intermediate‐sized S. alpinus (200–350 mm), however, suggested exploitation of the increase in the abundance of pelagic zooplankton in the late open‐water season. The results suggest that, in general, a strong littoral reliance of fishes can be a feature in subarctic lakes throughout the year. Due to its faster isotopic turnover rate and thus higher resolution for temporal diet changes, liver could be more commonly used in stable‐isotope studies of fish trophic niche shifts instead of using only the less responsive muscle tissue.     

A seasonal study of the carbon content of planktonic naked amoebae in the Hudson Estuary and in a productive freshwater pond with comparative data for ciliates

The total carbon contents of gymnamoebae and ciliates, dwelling in the water column of the Hudson Estuary and a highly productive freshwater pond, were monitored during a 7-month period from April through October 2006. The carbon contents of the gymnamoebae and the ciliates were greater in the pond compared with the estuary, and carbon contents of gymnamoebae were greater in the spring and autumn in both locations than those of ciliates. Given the global distribution of gymnamoebae, these results suggest that greater attention should be given to the potential role of gymnamoebae in microbial food webs.     

Microbial populations in acid mineral bioleaching systems of Tong Shankou Copper Mine, China

AIMS: To understand the composition and structure of microbial communities in different acid mineral bioleaching systems, and to present a more complete picture of microbially mediated acid mine drainage production. METHODS AND RESULTS: In Tong Shankou Copper Mine, China, two samples (named K1 and K2) from two different sites with bioleaching were studied. A bacterial 16S rDNA library and an archaeal 16S rDNA library of the sample from each site were constructed by 16S rDNA polymerase chain reaction (PCR), restriction fragment length polymorphism (RFLP) and sequencing. A total of 18 bacterial representative sequences and 12 archaeal representative sequences were obtained. Phylogenetic analysis indicated that 77.09% of the total bacterial clones were affiliated with Proteobacteria, and 21.22% of the total bacterial clones were closely related to Nitrospira. The rest of the bacterial clones were related to Firmicutes (1.68%). Sequences affiliated with the archaea of the Thermoplasma and Ferroplasma lineages were detected abundantly in the two samples. Unexpectedly, sequences affiliated with Sulfolobales and Methanothermus genera were also detected. CONCLUSIONS: The molecular studies appear to be consistent with the environmental conditions existing at the sites, which coincides with previous studies. High concentrations of some elements (such as copper, iron and sulfur) seemed to be the key factors resulting in the diverse distribution of typical iron-oxidizing bacteria such as Leptospirillum species and Acidithiobacillus ferrooxidans. SIGNIFICANCE AND IMPACT OF THE STUDY: Research on micro-organisms present in bioleaching systems especially archaea is not abundant. The acidophiles in the two bioleaching sites obtained from Tong Shankou Copper Mine, China, have not been reported until now. These results may expand our knowledge of the microbial diversity in the acid mineral bioleaching systems.     

Abundance of Naked Amoebae in Sediments of Hiroshima Bay, Seto Inland Sea of Japan

ABSTRACT The present paper provides the first data on naked amoebae from sediments of Hiroshima Bay. Three stations in the inner part of the bay were sampled over a three-month period. Abundance of naked amoebae ranged from 1,019 to 45,561 cells/g dry sediment. Results indicate: (i) surface sediment populations in most cases were higher than subsurface populations; (ii) there was some evidence of temporal variation with counts generally increasing from March to May: and (iii) the site located near Hiroshima City had fewer amoebae on several occasions than the other two sites. There was a negative exponential relationship between acid-volatile sulfide concentration and abundance of amoebae. Most amoebae were small with the average size ranging from 6.6–14 μm. Morphotype 1, amoebae that extend lobose pseudopodia or subpseudopodia during normal locomotion, were dominant (40–100% of enumerated amoebae). Morphotypes 2 and 3 (limax amoebae) were found in lower numbers than the other two morphotypes. The proportion of amoebae occupied by Morphotype 4 (fan-shaped or discoidal-flattened amoebae) was higher at a lower total abundance.     

Temporal and Spatial Abundance of Naked Amoebae (Gymnamoebae) in Marine Benthic Sediments of the Clyde Sea Area, Scotland

ABSTRACT. The abundances of benthic naked amoebae in the sediments of the Clyde Sea Area, Scotland, were studied throughout 1991. Four sites differing in sediment grain size and organic carbon content were chosen for study. Amoebae were enumerated by enrichment cultivation methods and found to be numerically important, attaining densities of up to 14,883 amoebae/cm³ on one occasion. They were most abundant, and temporally stable, in finer sediments where they averaged 2,224 cells/cm³ and lower and more variable in the sandy sediments, averaging 874 cells/cm³ throughout the year. In general, amoebae were most abundant in the surface sediment layers. Around 70 different morphotypes were recorded, and 61% of all amoebae counted were less than 10 μm in length. This is the first detailed quantitative study of benthic marine gymanamoebae and shows that naked amoebae and flagellates are numerically the dominant interstitial fauna in sediments of this area. Moreover, the gymnamoebae comprised the largest proportion of total protozoan biomass (excluding foraminiferans) and clearly need to be considered in future models of benthic carbon flow.     

Comparison of the Levels of Bacterial Diversity in Freshwater,Intertidal Wetland,and Marine Sediments by Using Millions of Illumina Tags

Sediment, a special realm in aquatic environments, has high microbial diversity. While there are numerous reports about the microbial community in marine sediment, freshwater and intertidal sediment communities have been overlooked. The present study determined millions of Illumina reads for a comparison of bacterial communities in freshwater, intertidal wetland, and marine sediments along Pearl River, China, using a technically consistent approach. Our results show that both taxon richness and evenness were the highest in freshwater sediment, medium in intertidal sediment, and lowest in marine sediment. The high number of sequences allowed the determination of a wide variety of bacterial lineages in all sediments for reliable statistical analyses. Principal component analysis showed that the three types of communities could be well separated from phylum to operational taxonomy unit (OTU) levels, and the OTUs from abundant to rare showed satisfactory resolutions. Statistical analysis (LEfSe) demonstrated that the freshwater sediment was enriched with Acidobacteria, Nitrospira, Verrucomicrobia, Alphaproteobacteria, and Betaproteobacteria. The intertidal sediment had a unique community with diverse primary producers (such as Chloroflexi, Bacillariophyta, Gammaproteobacteria, and Epsilonproteobacteria) as well as saprophytic microbes (such as Actinomycetales, Bacteroidetes, and Firmicutes). The marine sediment had a higher abundance of Gammaproteobacteria and Deltaproteobacteria, which were mainly involved in sulfate reduction in anaerobic conditions. These results are helpful for a systematic understanding of bacterial communities in natural sediment environments.     

Abundance and production of bacteria, and relationship to phytoplankton production, in a large tropical lake (Lake Tanganyika)

1. Abundance and bacterial production (BP) of heterotrophic bacteria (HBact) were measured in the north and south basins of Lake Tanganyika, East Africa, during seasonal sampling series between 2002 and 2007. The major objective of the study was to assess whether BP can supplement phytoplankton particulate primary production (particulate PP) in the pelagic waters, and whether BP and particulate PP are related in this large lake. HBact were enumerated in the 0–100 m surface layer by epifluorescence microscopy and flow cytometry; BP was quantified using ³H‐thymidine incorporation, usually in three mixolimnion layers (0–40, 40–60 and 60–100 m). 2. Flow cytometry allowed three subpopulations to be distinguished: low nucleic acid content bacteria (LNA), high nucleic acid content bacteria (HNA) and Synechococcus‐like picocyanobacteria (PCya). The proportion of HNA was on average 67% of total bacterial abundance, and tended to increase with depth. HBact abundance was between 1.2 × 10⁵ and 4.8 × 10⁶ cells mL⁻¹, and was maximal in the 0–40 m layer (i.e. roughly, the euphotic layer). Using a single conversion factor of 15 fg C cell⁻¹, estimated from biovolume measurements, average HBact biomass (integrated over a 100‐m water column depth) was 1.89 ± 1.05 g C m⁻². 3. Significant differences in BP appeared between seasons, especially in the south basin. The range of BP integrated over the 0–100 m layer was 93–735 mg C m⁻² day⁻¹, and overlapped with the range of particulate PP (150–1687 mg C m⁻² day⁻¹) measured in the same period of time at the same sites. 4. Depth‐integrated BP was significantly correlated to particulate PP and chlorophyll‐a, and BP in the euphotic layer was on average 25% of PP. 5. These results suggest that HBact contribute substantially to the particulate organic carbon available to consumers in Lake Tanganyika, and that BP may be sustained by phytoplankton‐derived organic carbon in the pelagic waters.     

Bottom-up and top-down regulation of decomposition in a tropical forest

The soil nutrients, microbes, and arthropods of tropical forests are patchy at multiple scales. We asked how these three factors interact to generate patterns of decomposition in 450 100 cm² litterbags arrayed along a 50 m ridge top in a Panama rainforest. We tested top-down (via grazing by microbivores like collembola and diplopods) and bottom-up (via added N and P) effects on the decomposition of cellulose. By using a 1,000-fold gradient in mesh size we generated a two-fold gradient in arthropod grazing. Microbivore grazing first retarded then ultimately enhanced decomposition rates. Micropulses of N and P (simulating concentrated urine) enhanced neither decomposition rates nor microbivores but increased the abundance of predacious ants. Decomposition rates also varied across the ridge, and were lowest in a plot with the deepest litter and highest soil moisture. These data generate the working hypothesis that N and P cascade upward at grains of 100 cm² to enhance a major predator in the litter; predators then absorb any increases in microbivores attracted to the extra fungal growth. These population interactions are in turn embedded in mesoscale variability generated by individual tree canopies that drive changes in litter quality and soil moisture. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Biomass changes and trophic amplification of plankton in a warmer ocean

Ocean warming can modify the ecophysiology and distribution of marine organisms, and relationships between species, with nonlinear interactions between ecosystem components potentially resulting in trophic amplification. Trophic amplification (or attenuation) describe the propagation of a hydroclimatic signal up the food web, causing magnification (or depression) of biomass values along one or more trophic pathways. We have employed 3‐D coupled physical‐biogeochemical models to explore ecosystem responses to climate change with a focus on trophic amplification. The response of phytoplankton and zooplankton to global climate‐change projections, carried out with the IPSL Earth System Model by the end of the century, is analysed at global and regional basis, including European seas (NE Atlantic, Barents Sea, Baltic Sea, Black Sea, Bay of Biscay, Adriatic Sea, Aegean Sea) and the Eastern Boundary Upwelling System (Benguela). Results indicate that globally and in Atlantic Margin and North Sea, increased ocean stratification causes primary production and zooplankton biomass to decrease in response to a warming climate, whilst in the Barents, Baltic and Black Seas, primary production and zooplankton biomass increase. Projected warming characterized by an increase in sea surface temperature of 2.29 ± 0.05 °C leads to a reduction in zooplankton and phytoplankton biomasses of 11% and 6%, respectively. This suggests negative amplification of climate driven modifications of trophic level biomass through bottom‐up control, leading to a reduced capacity of oceans to regulate climate through the biological carbon pump. Simulations suggest negative amplification is the dominant response across 47% of the ocean surface and prevails in the tropical oceans; whilst positive trophic amplification prevails in the Arctic and Antarctic oceans. Trophic attenuation is projected in temperate seas. Uncertainties in ocean plankton projections, associated to the use of single global and regional models, imply the need for caution when extending these considerations into higher trophic levels.