Microbial response to the presence of invasive ctenophore Mnemiopsis leidyi in the coastal waters of the Northeastern Adriatic (original) (raw)
Related papers
2012
Increasing biomasses of gelatinous zooplankton presumably have major implications for the structure and function of marine food webs at large; however, current data on lower trophic levels are scarce, as most studies have focused on the immediate effects on zooplankton and fish larvae only. We examined the short-term impact of larvae and adults of the invasive ctenophore Mnemiopsis leidyi on a summer planktonic food web in the estuarine southern Baltic Sea, with special emphasis on the microbial loop. Grazing by M. leidyi reduced the mesozooplankton biomass, followed by increased dinoflagellate biomass in treatments with M. leidyi. While chlorophyll a increased most in the treatments with M. leidyi, small phytoplankton and ciliates decreased in all treatments. M. leidyi had a slight effect on bacterial abundance, but not on bacterial production, ectoenzymatic activities, or community composition. Undetectable levels of phosphate and a gradual accumulation of dissolved organic carbon during the experiment suggested a malfunctioning microbial loop scenario. The experiment shows that direct and indirect short-term effects of M. leidyi on the estuarine food web are limited to higher trophic levels and indicates that top-down and bottom-up consequences of M. leidyi expansions on the microbial loop will likely depend on local nutrient conditions. KEY WORDS: Bacterioplankton · Nanoflagellates · Microbial loop · Trophic levels · Ciliates · Baltic Sea
Marine ecology …, 1988
In an attempt to quantify the organic fluxes within the microbial loop of oligotrophic Mediterranean water, organic pools and production rates were monitored. The production of cyanobacteria and its dynamics dominated the overall productivity in the system. The largest standing stock was that of the bacterioplankton and its growth consumed 8.3 pg C 1-' d-', hence about 60 % of the primary production was required for bacterial growth. Using the MiniCap technique, we measured a predation on bacteria of 2 6 X 104 bacteria ml-' h-'. This was in good agreement with the bacterial production rate of 2.3 X 104 cells rnl-' h-' Thus, growth and predation were balanced for heterotrophic bacterioplankton. Almost all of this predation on bacteria was due to organisms passing a 12 vm Nuclepore filter. This raises the question of what mechanisms channel 60 % of primary production into bacteria. We therefore outlined a mass-balance model to illustrate routes that could explain this transfer. According to our model the main flux route is cyanobacteria and concomitantly consumed heterotrophic bacteria carbon into bacterivores. A substantial fraction of the bacterivore and the microplankton carbon is released by excretion and/or cell lysis, to be used by the heterotrophic bacterioplankton. About 86% of the autotrophic production is balanced by respiration due to heterotrophic bacteria and protozoa, leaving 6 % of the primary production to higher trophic levels. This scenario should apply to ecosystems where bacterial production rate is high and comparable to primary production, and the dominant primary producers are cyanobacteria. A significant fraction of the photosynthetically fixed carbon will be mineralized within a simple microbial loop, thus rendering it an energy sink in the foodweb.
Environmental Microbiology, 2010
October 2007. Two 18S rRNA gene clone libraries were constructed from samples collected in spring and summer, and weekly changes in the abundances of five phylogenetic groups were studied by fluorescence in situ hybridization with newly designed probes. Stramenopiles affiliated with MAST-6 and Pedinellales were most numerous in spring but rare in summer. Both groups formed short-lived blooms during a sudden drop of salinity due to riverine influx (from 7.1 to 6.2 practical salinity units). The analysis of food vacuole content suggested that MAST-6 nanoflagellates were herbivorous, whereas bacterivory was found both in plastidic and aplastidic pedinellid populations. Members of an uncultured lineage of aplastidic, bacterivorous cercozoans distantly related to Ebria tripartita were more abundant in summer when water temperatures exceeded 17°C. Multicellular trophonts and/or free-living single cell stages of two lineages of Group 1 parasitic Syndiniales (alveolates) were present in spring and early summer. One of these alveolate populations repeatedly peaked before and after the freshwater influx, but was conspicuously absent throughout the period of decreased salinity. Our results indicate that nanoflagellate populations in coastal surface waters may form short-lived blooms that can only be detected by high-frequency sampling, and that may be related both to seasonal development and to sporadic (e.g. mixing) events. In view of their trophic diversity we moreover suggest that nanoflagellates in eutrophic coastal waters should not be regarded as a single functional unit.
Journal of Geophysical Research, 2005
1] Heterotrophic nanoflagellates and ciliates and their herbivorous activity were studied within the framework of the Programme Océan Multidisciplinaire Méso Echelle (POMME) in the northeastern Atlantic between 16°-22°W and 38°-45°N during winter, spring, and late summer/autumn 2001. Ciliate ingestion rates of Synechococcus and eukaryotic algae were measured using fluorescently labeled prey. Heterotrophic nanoflagellate ingestion rates of Synechococcus and Prochlorococcus were also estimated. Heterotrophic nanoflagellate and ciliate standing stock within the surface layer (0-100 m) showed seasonal variation, with maximal values in spring (866 mg C m À2 and 637 mg C m À2 , respectively). Oligotrichs dominated the ciliate assemblages, except at one site visited during spring, where a tintinnid bloom was observed. Ingestion of photosynthetic cells less than 10 mm in size was positively correlated (r = 0.7, p < 0.05, n = 12) with primary production and accounted for 2-94% of this. Phytoplankton consumption reflected differences in the evolution of the phytoplankton bloom and in the structure of the microbial food web, both associated with the strong mesoscale hydrodynamic variability of the study area. In that context it is worthy to note that when tintinnids reached high abundances locally (1260 cells L À1 ), their impact as phytoplankton grazers was important and reached 69% of primary production. Generally, heterotrophic nanoflagellates and ciliates were relatively more important in determining the fate of phytogenic carbon during spring. Another interesting feature of primary production consumption was that during the autumn, when Prochlorococcus dominated the phytoplankton community, the protozoan grazing activity was ineffective in regulating the fate of primary producers. Citation: Karayanni, H., U. Christaki, F. Van Wambeke, M. Denis, and T. Moutin (2005), Influence of ciliated protozoa and heterotrophic nanoflagellates on the fate of primary production in the northeast Atlantic Ocean,
Limnology and …, 2001
Benthic nitrogen processes have received substantial attention because the release of nutrients from sediments can contribute to the requirements of pelagic primary production; their study can also give an estimation of the importance of the sediment as a source or a sink of nutrients. Concepción Bay is located in central Chile and is the largest (167.4 km 2 ) and most enclosed embayment on the Chilean coastline. The bay is characterized by a strong hydrographic variability produced by the spring/summer seasonal upwelling of Equatorial subsurface waters (ESSW), rich in nutrients (ϳ25 M NO 3 Ϫ ) and poor in oxygen (Ͻ44.6 M). The area was studied in order to understand the consequences of phytodetrital deposition and oxygen deficiency on the environment and benthic communities. The study was carried out by sampling at a single station (28-m depth) in the inner part of the bay during winter (June 1998) and spring/summertime (November 1998 and January and March 1999). It was focused on measurements of benthic nitrogen fluxes, sulfate reduction, and denitrification rates before and after a phytoplankton bloom. Additionally, samples from the flocculent layer and from a semipurified bacterial mat were incubated under controlled oxygen conditions to determine NH 4 ϩ production. NH 4 ϩ exchange showed a clear seasonal pattern, with influxes during the winter (Ϫ7.6 Ϯ 4.9 mmol m Ϫ2 d Ϫ1 ) and high effluxes during the summer (36.6 and 20.8 mmol m Ϫ2 d Ϫ1 ) when the accumulation of fresh organic matter (evidenced as chlorophyll a) produced a flocculent layer over the sediments. Besides natural hypoxia of the bottom water associated with ESSW, the large input of organic matter resulted in anoxia within the sediment, as a consequence of respiration processes, and an enhancement in sulfate reduction rates (up to 200 mmol m Ϫ2 d Ϫ1 ). The flocculent layer then provided a favorable environment for the extensive development of Beggiatoa spp. mats. Overall, during the sampling period, NO 3
Marine Ecology Progress Series, 2003
the dilution method. Four sets of experiments were carried out quarterly in order to assess the impact on communities of both phototrophic and heterotrophic prey. Four different trophic models were observed: during the autumn microzooplankton fed on small dinoflagellates, and phototrophic (PNAN) and heterotrophic nanoflagellates (HNAN), but not on the abundant bulk of diatoms. The entire initial HNAN standing stock was removed; we therefore did not observe any mortality of bacteria, whose biomass was the highest in the whole period. In late winter, the intense diatom bloom of Lauderia annulata remained almost untouched as the microzooplankton fed only on a less abundant small sized diatom (Chaetoceros). Microzooplankton also fed on HNAN, halving the mortality of bacteria induced by HNAN grazing only. In late spring, microzooplankton grazed effectively on a large array of prey (small diatoms, PNAN and HNAN). Reduction of bacterial mortality, exerted by microzooplankton through grazing on HNAN, was less evident, possibly due to direct microzooplankton grazing on bacteria. During the summer, we observed an intense grazing on bacteria by microzooplankton, which shifted from the usual nano-sized prey organisms, due to their extreme paucity, to bacteria. In conclusion, microzooplankton grazing was highly selective and variable due to the prey composition and to the predator community structure, which were investigated at the species to genus level. Microzooplankton was unable to control a bloom of large-sized diatoms, but showed a high level of control on most of the PNAN fractions. The result of this selection contributed significantly to the shaping of the phytoplankton community structure. Microzooplankton controlled HNAN biomass even more efficiently with relevant indirect effects on bacterial mortality.
Research Square (Research Square), 2020
Background: Characterising ecological relationships between viruses, bacteria, and phytoplankton in the ocean are critical to understanding the ecosystem, yet these relationships are infrequently investigated together. To understand the dynamics of microbial communities and environmental factors in harmful algal blooms (HABs), we examined the environmental factors and microbial communities during Akashiwo sanguinea HABs in the Jangmok coastal waters of South Korea by metagenomics. Results: Specific bacterial communities showed synergistic and antagonistic relationships with A. sanguinea bloom. Endoparasitic dinoflagellate Amoebophrya sp. 1 controlled the bloom dynamics, as an increase in their abundance was correlated with HAB decline. In the nucleocytoplasmic large DNA viruses, abundance of Pandoraviridae increased following an increase in HAB. Operational taxonomic units and environmental factors associated with A. sanguinea were also visualized by network analysis: A. sanguinea-Amoebophrya sp. 1 (r=0.81, Time-lag: 2 day) and A. sanguinea-Pandoravirus dulcis (0.64, 0 day) relationships showed close association. A. sanguinea-dissolved organic carbon and-dissolved inorganic phosphorus relationships were also very closely correlated (each 0 day timelag, respectively). Conclusions: Microbial communities and the environment dynamically and complexly changed in A. sanguinea bloom, and a rapid turnover of microorganisms could respond to ecological interactions. A. sanguinea bloom dramatically changes the environments through their exudation of dissolved carbohydrates by autotrophic processes, followed by changes in microbial communities involving host-specific viruses, bacteria, and parasitoids. Thus, microbial communities in HAB ecology are phytoplankton taxa form harmful algal blooms (HABs), which can adversely impact marine ecosystems and human health[3]. A vast majority of the known HABs are dinoflagellates[4], among which, Akashiwo sanguinea causes frequent blooms world-wide[5,6]. A. sanguinea produces surfactants that saturate the feathers of marine birds with water and cause severe hypothermia[7] and have also been related to fish kills and marine mammal strandings[8]. However, the environmental changes caused by these strategies in dissolved organic matters and specific nutrient sources of this bloom are still poorly understood. Marine microbial communities are diverse and support other marine organisms. Microbial communities, including viruses, bacteria, fungi, and some parasitic algae, have the potential to impact population dynamics of HAB organisms[9]. Viruses are the most common biological entities in the marine environment, which contribute significantly to the flux of energy and matter, and influence biogeochemical cycling[10]. Nucleocytoplasmic large DNA viruses (NCLDVs) infect both animals and unicellular eukaryotes[11]. Members of the Phycodnaviridae family are large icosahedral NCLDVs that are mostly known to infect eukaryotic algae[12]. However, each viral family has not yet been assigned a species-specific host group. For example, Mimiviridae infect Acanthamoeba and other protists serve as natural hosts[13], but members of this group have also been found to infect various phytoplankton species, recently. Thus, role of each group of the NCLDVs in host-specific infection is yet to be elucidated[13,14]. Interactions between phytoplankton and bacteria are important in shaping their environment, and consequently, the biogeochemical cycles[15]. Phytoplankton relies on bacteria to remineralise organic matter back to its inorganic substituents[16]. Recently, specific bacterial phylotypes have been detected in association with different microalgae. Yang et al.[17] reported species-specific relationships between bacterial communities and A. sanguinea bloom. In eukaryotic parasitoids, Amoebophrya sp. kills its host and controls the dinoflagellate bloom[18]. Amoebophrya sp. has relatively short generation time and high prevalence in nature[19,20]. Studies on the interaction between Amoebophrya sp. and A. sanguinea bloom as host are in the laboratory[19]; however, ecological species-specific host-parasitoid interactions are yet to be elucidated. Results Environmental characteristics during Akashiwo sanguinea bloom Variations were observed in the environmental characteristics of JBTMS from June 2016 to June 2017 (Supplementary Fig. 1). A. sanguinea bloom sustained for 44 days; it developed on October 31 st and declined on December 13 th , 2016 (Fig. 1). During this blooming period, the mean abundance of A. sanguinea was 542 cells mL-1 , with a maximum abundance of 2,935 cells mL-1 on November 18 th ; the water temperature gradually decreased, and A. sanguinea bloom rapidly declined below 16 ºC (after November 21 st). Dissolved silica (DSi) concentrations remained between 21.18 and 30.67 μM, and did not show a significant correlation with the abundance of A. sanguinea. Dissolved inorganic nitrogen (DIN) concentrations rapidly decreased at the beginning of A. sanguinea bloom and remained 6 between 1.19 and 2.87 μM. Dissolved inorganic phosphorus (DIP), dissolved organic carbon (DOC), and chlorophyll a concentrations showed similar changes following A. sanguinea bloom and were significantly correlated with change in A. sanguinea abundance. Daily monitoring of the JBTMS from November 14 th to December 26 th , 2017, showed that the dominant phytoplankton was Bathycoccus prasinos (Chlorophyta) (Supplementary Fig. 2). We also observed that the water temperature was lower in 2017 than in 2016, rising over 16 ºC for only two days in 2017. pH and dissolved oxygen (DO) concentration were also lower in 2017 than in 2016. DIN, DIP, and DOC concentrations did not change with B. prasinos abundance. Changes in the DIP concentration showed no significant correlation with B. prasinos. The indoor microcosm experiment showed environmental characteristics similar to those of the JBTMS in 2016 (Supplementary Fig. 3). A. sanguinea abundance decreased gradually with decreasing water temperature. Ammonia, DIP, and DOC concentrations and total bacterial abundance decreased with decreasing A. sanguinea abundance, and increased again because of the substance release caused by the destruction of A. sanguinea cells in a closed environment. Species-specific bacterial community during A. sanguinea bloom mNGS results for bacterial community in JBTMS are summarised in Supplementary Table 1. In 2016, the bacterial community was classified into four groups at 73 % similarity by non-metric multidimensional scaling (nMDS) analysis (Fig. 2a). Group I was associated with "before A. sanguinea bloom" (4 th and 31 st October). This group comprised communities of Alpha-proteobacteria (73 %), Flavobacteriia (13 %), Gamma-proteobacteria (8 %), and other bacteria. Group II and III were associated with "during A. sanguinea bloom" (November 7 th to 28 th), wherein Flavobacteriia increased rapidly to 39.94 %. Group IV was associated with "after A. sanguinea bloom" (29 th November to 26 th December). In this group, abundance of Gamma-proteobacteria (13 %) increased from that of Group III. In 2017, bacterial community was divided into two groups at 70 % similarity by nMDS analysis (Fig. 2b). Group I was associated with "dominance of B. prasinos" (14 th November to 13 th December), and the group also comprised Alpha-proteobacteria (44 %), Flavobacteriia (20 %), Contributions
Aquatic Microbial Ecology, 2008
The grazing effect of heterotrophic nanoflagellates (HNF) and ciliates on bacterial production (BP), as well as their growth rates, was studied in winter, spring and autumn 2001 during the French research project Programme Océan Multidisciplinaire Méso-Echelle (POMME) in the northeast Atlantic Ocean (38 to 45°N, 16 to 22°W). The variability of different parameters studied appears to be largely controlled by the seasonal and latitudinal gradients of primary production rather than the strong eddy activity at the mesoscale level in the area. Heterotrophic microbial abundance, biomass and protistan grazing varied temporally, presenting highest values during the phytoplankton bloom, during the spring period and following the northward propagation of the bloom. HNF biomass integrated over the upper 100 m was highest in spring (270 to 850 mg C m-2). Ciliate integrated biomass was generally ≤160 mg C m-2 except in a Tintinnus sp. bloom in a northern anticyclonic eddy (A1) in spring when it reached 637 mg C m-2. HNF and ciliate growth rates varied from 0.2 to 0.7 d-1 and 0.2 to 1.4 d-1 , respectively. The fraction of BP consumed by ciliates was generally <10% except in the anticyclonic eddy A1 in spring during a tintinnid bloom when it reached 37% of BP. In conclusion, our data revealed that HNF can remove a large fraction of bacterial production in the northeast Atlantic Ocean (83 ± 27%, average of all sampling sites and seasons). Ciliates transferred less carbon to higher trophic levels than did HNF; however, episodic high occurrence of large bacterivorous ciliates, primarily tintinnids, increased the role of theses organisms as Clinks in the microbial food web.
Journal of Plankton Research, 2001
In a large number of marine systems, picoplankton is the dominant component of the planktonic food webs. Picoplanktonic organisms are a diverse group united only by size (<2 µm). This group includes heterotrophic bacteria, two types of photosynthetic prokaryotes, Synechococcus (Johnson and Sieburth, 1979) and Prochlorococcus (Chisholm et al., 1988) and some protists. Synechococcus and Prochlorococcus reach division rates of one division per day (Vaulot et al., 1995), while heterotrophic bacteria grow usually more slowly, with a generation time up to several days (Kirchman et al., 1995). Nevertheless, heterotrophic and autotrophic bacteria show a stable coexistence over large timescales (Landry et al., 1996). Heterotrophic bacteria are generally the most abundant component of the 0.2-2 µm size fraction and are the major contributors in carbon and nutrient cycling [(Fogg, 1995; Gasol et al., 1997) and references therein]. The photosynthetic prokaryotes Synechococcus and Prochlorococcus often dominate phytoplankton assemblages in terms of abundance and contribution to primary productivity (Glover et al., 1986; Chisholm et al., 1988; Weisse 1993). Heterotrophic nanoflagellates (HN) are typically recognized as the dominant picoplankton consumers in oceanic systems [e.g. (Fenchel, 1982a, 1982b; Reckermann and Veldhuis, 1997; Sanders et al., 1992, 2000)]. Despite their significance, several aspects of loss processes of picoplankters in situ have not been elucidated. First, concerning the grazing of heterotrophic bacteria, some uncertainty still exists due to the fact that common methodological approaches have a number of drawbacks which may lead to under-or overestimation of grazing [e.g.
Marine Ecology Progress Series, 2001
The variability in microbial communities (abundance and biomass), bacterial production and ectoaminopeptidase activity, particulate and dissolved organic carbon (POC, DOC), and particulate and dissolved lipids was examined in spring 1995 in the northwestern Mediterranean, where a transition from the end of a bloom to pre-oligotrophic conditions was observed. Four time series of 36 h each and 4 h sampling intervals were performed at 5 m and at the chlorophyll maximum (30 m) between 11 and 31 May. Simultaneous measurements of pigments, abundance of hetero-and autotrophic flagellates, bacteria and POC enabled the estimation of living POC (defined as autotrophic-C plus heterotrophic-C biomass), and thus the detrital organic carbon. During the first 2 time series (11 to 15 May), the bacterial-C biomass was higher than the autotrophic-C biomass at 5 m (ratio 1.4 and 1.7), whereas the opposite trend was observed in the chlorophyll peak (ratio 0.7 for the first cycle). However, at the end of May, autotrophic-C biomass was equivalent to bacterial-C biomass at both depths studied. The detrital pool remained a more or less constant fraction of the POC (52, 53 and 47% on 11-12 May, 14-15 May and 30-31 May) at the chlorophyll peak, whereas it decreased significantly with time (62 to 53%) at 5 m. Relationships between bacterial activities and evolution of available resources were not systematically evidenced from our 36 h diel cycle data. Nevertheless, at the monthly scale, comparison of bacterial carbon demand (BCD) to potential carbon resources (detrital POC and DOC) showed that bacteria fed differently on the various pools. From ectoaminopeptidase turnover rates and detrital POC, the potential hydrolysis rate of detritus was calculated. Depending on the choice of conversion factors for bacterial production and estimates of hydrolysis turnover rates, it was shown that bacterial hydrolysis of detritus could be one of the DOC accumulation sources. We observed that the percentage of BCD supplied by detrital POC hydrolysis increased in the surface and decreased in the chlorophyll peak. An index of lipid degradation in POC, the lipolysis index, increased during the month at 5 m, also indicating a higher hydrolysis of POC. The opposite trend was observed in the chlorophyll maximum layer. The selective decrease in dissolved lipids in DOC in the chlorophyll maximum layer, particularly free fatty acids, also suggests that bacteria utilized increased fractions of carbon sources from the DOC. We concluded that partitioning between DOC and detritus as resources for bacteria can change during the rapid transition period from mesotrophy to oligotrophy in the northwestern Mediterranean.