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Our study on a shallow tropical lake identified fluctuations and interactions of rotifer assemblage, based on trophic guild analysis, comparable to those found in temperate lakes. We also highlighted that trophic guilds, based on trophi structure, has broad application to both temperate and tropical water bodies, which shows the universality of this approach. In addition, our analysis on the interaction between the exotic species Kellicottia bostoniensis and other microphagous rotifers were sufficient to demonstrate that it does not have invasive characteristics.
The Guild Ratio (GR), based on the density of raptorial and microphagous functional groups of rotifers, revealed to be an appropriate tool in the evaluation of possible interactions with other planktonic groups, as well as in the evaluation of temporal changes of functional groups. Unlike Obertegger and Manca5 and Obertegger et al.11, we used the database of densities of functional groups instead of biomass, according to Smith et al.10. The significant correlation between GR and cladocerans showed that GR, based on number of individuals, indicated interaction between microphagous rotifers and cladocerans like that reported by Obertegger and Manca5 and Obertegger et al.11 in temperate lakes, based on biomass (GR′). The relationship GR-cladocerans showed a similar trend with monthly and bimonthly data, indicating its adequacy even when data are less frequently obtained, which agrees with results from Obertegger et al.11 in Lake Washington, USA. Given this point, our findings reinforce that other studies may be designed with lower sampling frequency and certainly achieve satisfactory results, allowing a cheaper logistic planning in further research.
The significant positive correlation between GR and cladoceran densities indicates competition between the groups, corroborating the initial hypothesis. The predominance of microphagous rotifers (i.e. lower GR values) when cladoceran densities decreased, represented mainly by Daphnia gessneri (max. size 1.22 mm) and Ceriodaphnia richardi (max. 0.70 mm)29, is a sign of competition between both groups. Therefore, when cladocerans were more abundant during the cool season (May–September), the raptorial rotifers species predominated, which coexist with filtering cladocerans, similarly to results obtained by Obertegger et al.11, in lakes Washington (USA) and Caldonazzo (Italy). Exploitative competition between cladocerans and rotifers, particularly microphagous species, which occupy a similar niche, may even lead to competitive exclusion of rotifers. Herbivorous cyclopoid nauplii could compete with rotifers and make our analysis meaningful, however there was no evidence of interaction between them and microphagous rotifers, which does not support our hypothesis.
Several studies report the competitive superiority of cladocerans4,30,31. The inferiority of rotifers may be partly due to lower clearance rate (1–10 µL ind.−1 h−1) than cladocerans (10–150 µL ind.−1 h−1) as well as a more limited size food range (ca. 4–17 µm)1. The maximum clearance rate of cladocerans may be much higher than that already mentioned by Nogrady et al.1 and dependent on various factors such as temperature, food concentration and body size9. Rotifer populations may be suppressed by more efficient cladocerans through exploitative competition, although rotifers may also suffer effects from interference competition32,33. Cladocerans larger than 1.2 mm may suppress small rotifer populations by interference34. In Lake Monte Alegre, cladoceran species are relatively small and probably exploitative competition is the most important interaction in this community.
The increase in algal carbon and temperature in the Lake Monte Alegre during the warm season (October–April) was not followed by increase of the total rotifer densities, indicating a preponderant influence of another factor. However, as mentioned above, there was an increase in the abundance of microphagous species and a decrease in densities of raptorial species in this season. Raptorial species, particularly large species (e.g., Synchaeta spp.), prefer larger items ( > 50 µm) such as algae, ciliates and other rotifers13. Species of the genus Ascomorpha feed on dinophytes, such as Peridinium and Ceratium, which are grasped, and the content sucked1. In Lake Monte Alegre, an increase of Peridinium in the fall and winter (March–September) was already reported35,36, which would benefit some raptorial rotifers, including Ascomorpha. However, in this study in 2011–2012, dinophytes were not abundant (L.H.S. Silva, unpublished data), representing about 1.4% of the total phytoplankton density, chlorophytes predominating, increasing the contribution of cyanobacteria in the warm season. Therefore, higher densities of raptorial species in the cool season were unrelated to phytoplankton composition and, on the other hand, higher temperatures in the warm season did not favor the increase in populations of this group.
The distribution of organisms can be a strategy to avoid competition and predation. In Lake Monte Alegre, several species of Colotheca, Keratella, Polyarthra, and Trichocerca occupied the entire water column in the cool season (A. J. Meschiatti et al. unpublished data). In the warm season, species of these genera, in addition to Brachionus, Hexarthra and Ptygura were limited to the oxygenated layer, avoiding the anoxic hypolimnion. Another feature of the vertical distribution of rotifers in this lake was the frequent occupation of the most superficial layer, even during the day, which is rarely occupied by cladocerans37, reducing overlap and possible interactions with other organisms.
Direct predation on rotifers by chaoborid larvae is low in Lake Monte Alegre, representing 9% of the prey number for instars I and II, 4% for instar III, not being preyed on by instar IV38. In an experiment with mesocosm in this lake, no predation effect by Chaoborus larvae on Keratella spp. densities was detected39. Zooplankton predation by fish in the lake is mainly exerted by adult of the exotic cichlid Tilapia rendalli (current name Coptodon rendalli), a pump filter-feeder40, which collects organisms with lower evasion to the filtering current, which, however, are not abundant in the lake. Although Keratella sp. was not rejected by tilápia, its consumption is low by this fish species, whose predation is higher on cladocerans40.
Temporal variations of functional groups of rotifers in Lake Monte Alegre indicated the indirect effect of cladoceran predation by invertebrates, such as Chaoborus brasiliensis larvae and the aquatic mite, Krendowskia sp., in 2011–201241. Predation pressure by invertebrates is generally higher in the warm season when their populations increased, resulting in declining cladoceran populations29,41. Consequently, there is a decrease in exploitative competition by cladocerans and the possibility of competitive exclusion when resources are limiting. Predation by invertebrates has emerged as the main structuring factor of the lake zooplankton29, and this study highlights the indirect effect of this factor on rotifers.
The high frequency of occurrence of the exotic species Kellicottia bostoniensis in the present study, combined with the weekly sampling strategy adopted, demonstrates the great persistence capacity of this species in the environment, with rare occasions when it is excluded from the water column. This feature indicates success of the exotic species in the new habitat22. The characteristics of an invasive species are not always scientifically proven, and many failures are not reported in publications, introducing a bias in evaluating the success of exotic species19. The presence of this exotic species in Lake Monte Alegre had not been detected in previous studies conducted in the 1980s42,43. Although very common, according to Josefsson and Andersson18 it is not invasive in the lake, as it did not constitute a threat to the local community of rotifers. It does not outcompete other microphagous rotifers and, on the contrary, there is evidence of being competitively inferior, as its population decreased in periods of dominance of other microphagous species. A laboratory experiment showed that K. bostoniensis had no effect on zooplankton composed of native copepods, cladocerans, and rotifers, affecting only ciliates, which are part of its food resources23, reinforcing the idea that it does not constitute a threat to the whole planktonic community.
This exotic species was caught in lakes from River Doce valley44 and in Furnas Reservoir45, in Brazil, at lower densities than those of Lake Monte Alegre (max. 127 ind. L−1). The vertical distribution in Nado Reservoir, located in Brazil, showed its highest abundance in the anoxic hypolimnion, on a diel cycle46, indicating resistance of this species to adverse conditions. In some Swedish lakes, the exotic species K. bostoniensis was also found in deeper layers18, as well as in Mirror Lake, United States, where the production of K. bostoniensis, a native species, was higher at the bottom47. Apparently, this species maintains similar distribution in its original habitat and a new habitat. The ability to occupy lower layers, often anoxic, where few microcrustaceans and rotifers are found, would lower negative interactions with other populations and even constitutes a defense strategy against predation by most invertebrates and filtering fish48. More

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To expand on previous BONCAT findings, we initially performed an experiment with E. coli, which demonstrated that translational activity as measured by BONCAT can only be detected when cultures were grown with glucose or sorbitol as the sole carbon and energy source but not with sucrose (Supplementary Fig. 1). This is consistent with the notion that E. coli is genetically incapable of sucrose utilization. Addition of chloramphenicol, an antibiotic targeting ribosome function, to the culture decreased the BONCAT fluorescence intensity to background levels, i.e., fluorescence values observed when cells were grown with HPG but without growth substrate. These results demonstrated that BONCAT can be used to study cell activity responses to substrate amendment and suggested that it could be used to study complex microbiomes.
For this benchmark study, we selected a high temperature (74 °C), alkaline (pH 8.2) hot spring (Five Sisters 5, FS5) in the Lower Geyser Basin of YNP (Fig. 1). Hot springs harbor lower complexity microbial communities compared to other environments, such as soils and marine sediments, making them an ideal system for the development of novel approaches. As indicated by 16S rRNA gene amplicon sequencing, hot spring FS5 was dominated by the archaeal candidate phylum Aigarchaeota (41.9%), with the next most abundant community members belonging to bacterial candidate phylum Fervidibacteria (9.57%) and phylum Deinococcus-Thermus (7.98%) (Fig. 2). Members of the Aigarchaeota have been detected in many high temperature (65–88 °C) hot springs over a wide pH range (2.9–9.3) [25]. Despite multiple studies describing their versatile metabolic potential, Aigarchaeota remain recalcitrant to cultivation and no experimental data on their functional activity are currently available. Reconstructed genomes suggest the capacity for aerobic respiration or anaerobic respiration with nitrate as an electron acceptor [25]. In addition, a recent study found multiple endoglucanases and β-glucosidases that might be involved with degradation of cellulose and cellobiose in an Aigarchaeota metagenome bin [26]. One of the goals of our study was to test these functional predictions using BONCAT-FACS.
Fig. 2: 16S rRNA gene relative abundances in averaged incubations.

Top panel, unamended FS5 community at the time of sampling (T0). Middle panel, community composition of presort samples, representing the extractable microbial community, after the incubation experiments. Bottom panel, composition of the sorted active cell fraction after incubation with substrate amendment. Only taxa that were represented above 1% in at least one sample are shown. Additional taxa were combined into “Other” category. Taxon level represents highest taxonomic resolution for each taxa (Silva 128). Some replicates did not pass the quality control steps of our bioinformatics pipeline (1% relative abundance of the total extractable community, ASVs collapsed to the genus level) were active in at least one condition, and most taxa were active under several conditions (Fig. 2). This demonstrates that BONCAT can be applied to a wide variety of phylogenetic groups, which is consistent with previous reports [5,6,7,8,9, 27]. The sorted, active fraction from incubations with different treatments contained no statistically significant difference when compared to the HPG-only control based on Bray–Curtis dissimilarity (MANOVA, p = 1) (Fig. 2). This result indicates that the microbial activity response to any treatment, as captured by BONCAT, was not large enough or consistent enough among replicates to significantly change the overall active community when compared to the HPG-only control.
Although the overall composition of the active communities did not vary significantly in response to incubation conditions, changes within the richness and evenness of the communities were detected. To further describe the community composition, the Shannon’s diversity index of each incubation was calculated (Fig. 3). For each treatment, the bulk, presort fraction (representing the total, extractable cell community), and the sorted, active cell fraction were analyzed and compared to the respective HPG-only control. Overall, the variation in the presort fraction of Shannon’s diversity indices was less variable than the sorted fraction from the same treatment incubation (Fig. 3). This demonstrated that the BONCAT-FACS approach could detect changes in the diversity of the active community due to individual cell responses prior to shifts in cell abundance occurring in presort communities. We expected little variation in the presort community because the limited time of incubation should not have allowed for an overall shift in community composition on a bulk level. However, Fervidibacteria were observed in higher proportion in most presort populations as compared to the original T0 bulk sample. This could be attributed to either favorable growth of this yet uncultured lineage or be a result of preferential cell extraction or cell lysis during freeze–thaw cycles as compared to bulk sample DNA extraction. Alternatively, their increase in relative abundance could have resulted from sample cooling (72 to 55 °C) during transit from the field to the laboratory (4 h).
Fig. 3: Change in Shannon’s diversity indices of each treatment standardized to HPG-only controls.

The Shannon’s diversity indices for presort and sorted samples were compared relative to their respective HPG-only controls. The value for HPG-only was set to 0 and the difference for each sample is plotted. Overall, presort samples exhibited less variability than sorted samples. Sorted samples for cellobiose and anoxic conditions (100% N2 headspace) were significantly different from the sorted HPG-only (atmospheric air) control (p  More

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