Impacts of an invasive filter-feeder on bacterial biodiversity are context dependent.

Bacteria represent most of the biodiversity and play key roles in virtually every ecosystem. In doing so, bacteria act as part of complex communities shaped by interactions across all domains of life. Here, we report on direct interactions between bacteria and dreissenid mussels, a group of invasive filter-feeders threatening global aquatic systems due to high filtration rates. Previous studies showed that dreissenids can impact bacterial community structure by changing trait distributions and abundances of specific taxa. However, studies on bacterial community effects were conducted using water from Lake Michigan (an oligotrophic lake) only, and it is unknown whether similar patterns are observed in systems with differing nutrient regimes. We conducted ten short-term dreissenid grazing experiments in 2019 using water from two eutrophic lake regions-the western basin of Lake Erie and Saginaw Bay in Lake Huron. Predation by dreissenids led to decline in overall bacterial abundance and diversity in both lakes. However, feeding on bacteria was not observed during every experiment. We also found that traits related to feeding resistance are less phylogenetically conserved than previously thought. Our results highlight the role of temporal, spatial, and genomic heterogeneity in bacterial response dynamics to a globally important invasive filter feeder.

Comparative analysis of Microcystis buoyancy in western Lake Erie and Saginaw Bay of Lake Huron.

Microcystis is the predominant genus of harmful cyanobacterium in both Lake Erie and Saginaw Bay of Lake Huron and has the capacity to regulate the buoyancy of its colonies, sinking under certain conditions while floating towards the surface in others. Understanding the factors that control buoyancy is critical for interpretation of remote sensing data, modeling and forecasting harmful algal blooms within these two systems. To determine if Microcystis colony buoyancy in the two lakes responds similarly to diurnal light cycles, colony buoyant velocity (floating/sinking terminal velocity in a quiescent water column) and size were measured after manipulating the intensity of sunlight. Overall, there were more positively buoyant (floating) colonies in Lake Erie while most of the colonies in Saginaw Bay were negatively buoyant (sinking). In Lake Erie the colonies became less buoyant at increased light intensities and were less buoyant in the afternoon than in the morning. In both lakes, apparent colony density was more variable among small colonies (< 200 µm), whereas larger colonies showed a diminished response of density to light intensity and duration. These findings suggest that colony density becomes less plastic as colonies increase in size, leading to a weak relationship between size and velocity. These relationships may ultimately affect how the bloom is transported throughout each system and will help explain observed differences in vertical distribution and movement of Microcystis in the two lakes.

The genetic and ecophysiological diversity of Microcystis.

Microcystis is a cyanobacterium that forms toxic blooms in freshwater ecosystems around the world. Biological variation among taxa within the genus is apparent through genetic and phenotypic differences between strains and via the spatial and temporal distribution of strains in the environment, and this fine-scale diversity exerts strong influence over bloom toxicity. Yet we do not know how varying traits of Microcystis strains govern their environmental distribution, the tradeoffs and links between these traits, or how they are encoded at the genomic level. Here we synthesize current knowledge on the importance of diversity within Microcystis and on the genes and traits that likely underpin ecological differentiation of taxa. We briefly review spatial and environmental patterns of Microcystis diversity in the field and genetic evidence for cohesive groups within Microcystis. We then compile data on strain-level diversity regarding growth responses to environmental conditions and explore evidence for variation of community interactions across Microcystis strains. Potential links and tradeoffs between traits are identified and discussed. The resulting picture, while incomplete, highlights key knowledge gaps that need to be filled to enable new models for predicting strain-level dynamics, which influence the development, toxicity and cosmopolitan nature of Microcystis blooms.

Environmental (e)RNA advances the reliability of eDNA by predicting its age.

Environmental DNA (eDNA) analysis has advanced conservation biology and biodiversity management. However, accurate estimation of age and origin of eDNA is complicated by particle transport and the presence of legacy genetic material, which can obscure accurate interpretation of eDNA detection and quantification. To understand the state of genomic material within the environment, we investigated the degradation relationships between (a) size of fragments (long vs short), (b) genomic origins (mitochondrial vs nuclear), (c) nucleic acids (eDNA vs eRNA), and (d) RNA types (messenger (m)RNA vs ribosomal (r)RNA) from non-indigenous Dreissena mussels. Initial concentrations of eRNA followed expected transcriptional trends, with rRNAs found at > 1000 × that of eDNA, and a mitosis-associated mRNA falling below detection limits within 24 h. Furthermore, the ratio of eRNA:eDNA significantly decreased throughout degradation, potentially providing an estimate for the age of genomic material. Thus, eRNA quantification can increase detection due to the high concentrations of rRNAs. Furthermore, it may improve interpretation of positive detections through the eRNA:eDNA ratio and/or by detecting low abundant mitosis-associated mRNAs that degrade within ~ 24 h.

Flow cytometric monitoring of bacterioplankton phenotypic diversity predicts high population-specific feeding rates by invasive dreissenid mussels.

Species invasion is an important disturbance to ecosystems worldwide, yet knowledge about the impacts of invasive species on bacterial communities remains sparse. Using a novel approach, we simultaneously detected phenotypic and derived taxonomic change in a natural bacterioplankton community when subjected to feeding pressure by quagga mussels, a widespread aquatic invasive species. We detected a significant decrease in diversity within 1 h of feeding and a total diversity loss of 11.6 ± 4.1% after 3 h. This loss of microbial diversity was caused by the selective removal of high nucleic acid populations (29 ± 5% after 3 h). We were able to track the community diversity at high temporal resolution by calculating phenotypic diversity estimates from flow cytometry (FCM) data of minute amounts of sample. Through parallel FCM and 16S rRNA gene amplicon sequencing analysis of environments spanning a broad diversity range, we showed that the two approaches resulted in highly correlated diversity measures and captured the same seasonal and lake-specific patterns in community composition. Based on our results, we predict that selective feeding by invasive dreissenid mussels directly impacts the microbial component of the carbon cycle, as it may drive bacterioplankton communities toward less diverse and potentially less productive states.

Lake Bacterial Assemblage Composition Is Sensitive to Biological Disturbance Caused by an Invasive Filter Feeder.

One approach to improve forecasts of how global change will affect ecosystem processes is to better understand how anthropogenic disturbances alter bacterial assemblages that drive biogeochemical cycles. Species invasions are important contributors to global change, but their impacts on bacterial community ecology are rarely investigated. Here, we studied direct impacts of invasive dreissenid mussels (IDMs), one of many invasive filter feeders, on freshwater lake bacterioplankton. We demonstrated that direct effects of IDMs reduced bacterial abundance and altered assemblage composition by preferentially removing larger and particle-associated bacteria. While this increased the relative abundances of many free-living bacterial taxa, some were susceptible to filter feeding, in line with efficient removal of phytoplankton cells of <2 µm. This selective removal of particle-associated and larger bacteria by IDMs altered inferred bacterial functional group representation, defined by carbon and energy source utilization. Specifically, we inferred an increased relative abundance of chemoorganoheterotrophs predicted to be capable of rhodopsin-dependent energy generation. In contrast to the few previous studies that have focused on the longer-term combined direct and indirect effects of IDMs on bacterioplankton, our study showed that IDMs act directly as a biological disturbance to which freshwater bacterial assemblages are sensitive. The negative impacts on particle-associated bacteria, which have been shown to be more active than free-living bacteria, and the inferred shifts in functional group representation raise the possibility that IDMs may directly alter bacterially mediated ecosystem functions. IMPORTANCE Freshwater bacteria play fundamental roles in global elemental cycling and are an intrinsic part of local food webs. Human activities are altering freshwater environments, and much has been learned regarding the sensitivity of bacterial assemblages to a variety of these disturbances. Yet, relatively few studies have focused on how species invasion, which is one of the most important aspects of anthropogenic global change, affects freshwater bacterial assemblages. This study focuses on the impact of invasive dreissenid mussels (IDMs), a globally distributed group of invasive species with large impacts on freshwater phyto- and zooplankton assemblages. We show that IDMs have direct effects on lake bacterioplankton abundance, taxonomic composition, and inferred bacterial functional group representation.

Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C1 Compound Oxidation.

The Chloroflexi CL500-11 clade contributes a large proportion of the bacterial biomass in the oxygenated hypolimnia of deep lakes worldwide, including the world's largest freshwater system, the Laurentian Great Lakes. Traits that allow CL500-11 to thrive and its biogeochemical role in these environments are currently unknown. Here, we found that a CL500-11 population was present mostly in offshore waters along a transect in ultraoligotrophic Lake Michigan (a Laurentian Great Lake). It occurred throughout the water column in spring and only in the hypolimnion during summer stratification, contributing up to 18.1% of all cells. Genome reconstruction from metagenomic data suggested an aerobic, motile, heterotrophic lifestyle, with additional energy being gained through carboxidovory and methylovory. Comparisons to other available streamlined freshwater genomes revealed that the CL500-11 genome contained a disproportionate number of cell wall/capsule biosynthesis genes and the most diverse spectrum of genes involved in the uptake of dissolved organic matter (DOM) substrates, particularly peptides. In situ expression patterns indicated the importance of DOM uptake and protein/peptide turnover, as well as type I and type II carbon monoxide dehydrogenase and flagellar motility. Its location in the water column influenced its gene expression patterns the most. We observed increased bacteriorhodopsin gene expression and a response to oxidative stress in surface waters compared to its response in deep waters. While CL500-11 carries multiple adaptations to an oligotrophic lifestyle, its investment in motility, its large cell size, and its distribution in both oligotrophic and mesotrophic lakes indicate its ability to thrive under conditions where resources are more plentiful. Our data indicate that CL500-11 plays an important role in nitrogen-rich DOM mineralization in the extensive deep-lake hypolimnion habitat.

AN "ENVIRO-INFORMATIC" ASSESSMENT OF SAGINAW BAY (LAKE HURON, USA) PHYTOPLANKTON: DATA-DRIVEN CHARACTERIZATION AND MODELING OF MICROCYSTIS (CYANOPHYTA)(1).

Phytoplankton and Microcystis aeruginosa (Kütz.) Kütz. biovolumes were characterized and modeled, respectively, with regard to hydrological and meteorological variables during zebra mussel invasion in Saginaw Bay (1990-1996). Total phytoplankton and Microcystis biomass within the inner bay were one and one-half and six times greater, respectively, than those of the outer bay. Following mussel invasion, mean total biomass in the inner bay decreased 84% but then returned to its approximate initial value. Microcystis was not present in the bay during 1990 and 1991 and thereafter occurred at/in 52% of sample sites/dates with the greatest biomass occurring in 1994-1996 and within months having water temperatures >19°C. With an overall relative biomass of 0.03 ± 0.01 (mean + SE), Microcystis had, at best, a marginal impact upon holistic compositional dynamics. Dynamics of the centric diatom Cyclotella ocellata Pant. and large pennate diatoms dominated compositional dissimilarities both inter- and intra-annually. The environmental variables that corresponded with phytoplankton distributions were similar for the inner and outer bays, and together identified physical forcing and biotic utilization of nutrients as determinants of system-level biomass patterns. Nonparametric models explained 70%-85% of the variability in Microcystis biovolumes and identified maximal biomass to occur at total phosphorus (TP) concentrations ranging from 40 to 45 µg · L(-1) . From isometric projections depicting modeled Microcystis/environmental interactions, a TP concentration of <30 µg · L(-1) was identified as a desirable contemporary "target" for management efforts to ameliorate bloom potentials throughout mussel-impacted bay waters.