Intense winter heterotrophic production stimulated by benthic resuspension

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/109851/1/lno20004571672.pd

Randomized lasso links microbial taxa with aquatic functional groups inferred from flow cytometry

High-nucleic-acid (HNA) and low-nucleic-acid (LNA) bacteria are two operational groups identified by flow cytometry (FCM) in aquatic systems. A number of reports have shown that HNA cell density correlates strongly with heterotrophic production, while LNA cell density does not. However, which taxa are specifically associated with these groups, and by extension, productivity has remained elusive. Here, we addressed this knowledge gap by using a machine learning-based variable selection approach that integrated FCM and 16S rRNA gene sequencing data collected from 14 freshwater lakes spanning a broad range in physicochemical conditions. There was a strong association between bacterial heterotrophic production and HNA absolute cell abundances (R-2 = 0.65), but not with the more abundant LNA cells. This solidifies findings, mainly from marine systems, that HNA and LNA bacteria could be considered separate functional groups, the former contributing a disproportionately large share of carbon cycling. Taxa selected by the models could predict HNA and LNA absolute cell abundances at all taxonomic levels. Selected operational taxonomic units (OTUs) ranged from low to high relative abundance and were mostly lake system specific (89.5% to 99.2%). A subset of selected OTUs was associated with both LNA and HNA groups (12.5% to 33.3%), suggesting either phenotypic plasticity or within-OTU genetic and physiological heterogeneity. These findings may lead to the identification of system-specific putative ecological indicators for heterotrophic productivity. Generally, our approach allows for the association of OTUs with specific functional groups in diverse ecosystems in order to improve our understanding of (microbial) biodiversity-ecosystem functioning relationships. IMPORTANCE A major goal in microbial ecology is to understand how microbial community structure influences ecosystem functioning. Various methods to directly associate bacterial taxa to functional groups in the environment are being developed. In this study, we applied machine learning methods to relate taxonomic data obtained from marker gene surveys to functional groups identified by flow cytometry. This allowed us to identify the taxa that are associated with heterotrophic productivity in freshwater lakes and indicated that the key contributors were highly system specific, regularly rare members of the community, and that some could possibly switch between being low and high contributors. Our approach provides a promising framework to identify taxa that contribute to ecosystem functioning and can be further developed to explore microbial contributions beyond heterotrophic production

Year-Round Measures of Planktonic Metabolism Reveal Net Autotrophy in Surface Waters of a Great Lakes Estuary

During 2009 and 2010, we quantified monthly changes in plankton metabolism and environmental variables in the surface waters of Muskegon Lake, a Great Lakes estuary connected to Lake Michigan. Muskegon Lake’s mean (±SE) annual gross plankton primary production (GPP) and respiration (R) rates were 46 ± 9 and 23 ± 4 mg C l−1 yr−1, respectively. GPP:R ratios of 0.6 to +4.8 with a yearly mean of 2.0 ± 0.3 indicated that the surface water of Muskegon Lake was net autotrophic during all but the winter months under ice cover, when it was in a near carbon balance to slightly heterotrophic state. Approximately 5% of GPP and 12% of R occurred during the winter months, highlighting winter’s potential role in nutrient regeneration. An overall positive annual net community production (NCP) rate of 28 ± 6 mg C l−1 yr−1 makes Muskegon Lake’s surface waters a net sink for carbon on an annual basis. Annual heterotrophic bacterial production (BP) rates were 5 ± 3 mg C l−1 yr−1, suggesting a substantial fraction of GPP was likely processed through the microbial food web (2 to 76%). A stepwise multiple linear regression model revealed the plausible drivers of GPP (temperature [T], photosynthetically active radiation [PAR], total phosphorus [TP], dissolved oxygen [DO], chlorophyll a [chl a]), NCP (T, PAR, TP), R (T, DO, ammonium [NH3], soluble reactive phosphorous [SRP], dissolved organic carbon [DOC]) and GPP:R (T, PAR, SRP, DOC). Year-round measurements inform us of the strong seasonality in the carbon cycle of temperate lakes

Seeking Sunlight: Rapid Phototactic Motility of Filamentous Mat-Forming Cyanobacteria Optimize Photosynthesis and Enhance Carbon Burial in Lake Huron’s Submerged Sinkholes

We studied the motility of filamentous mat-forming cyanobacteria consisting primarily ofOscillatoria-like cells growing under low-light, low-oxygen, and high-sulfur conditions in Lake Huron’s submerged sinkholes using in situ observations, in vitro measurements and time-lapse microscopy. Gliding movement of the cyanobacterial trichomes (100–10,000 μm long filaments, composed of cells ~10 μm wide and ~3 μm tall) revealed individual as well as group-coordinated motility. When placed in a petri dish and dispersed in ground water from the sinkhole, filaments re-aggregated into defined colonies within minutes, then dispersed again. Speed of individual filaments increased with temperature from ~50 μm min-1 or ~15 body lengths min-1 at 10∘C to ~215 μm min-1 or ~70 body lengths min-1 at 35∘C – rates that are rapid relative to non-flagellated/ciliated microbes. Filaments exhibited precise and coordinated positive phototaxis toward pinpoints of light and congregated under the light of foil cutouts. Such light-responsive clusters showed an increase in photosynthetic yield – suggesting phototactic motility aids in light acquisition as well as photosynthesis. Once light source was removed, filaments slowly spread out evenly and re-aggregated, demonstrating coordinated movement through inter-filament communication regardless of light. Pebbles and pieces of broken shells placed upon intact mat were quickly covered by vertically motile filaments within hours and became fully buried in the anoxic sediments over 3–4 diurnal cycles – likely facilitating the preservation of falling debris. Coordinated horizontal and vertical filament motility optimize mat cohesion and dynamics, photosynthetic efficiency and sedimentary carbon burial in modern-day sinkhole habitats that resemble the shallow seas in Earth’s early history. Analogous cyanobacterial motility may have played a key role in the oxygenation of the planet by optimizing photosynthesis while favoring carbon burial

Microhabitats are associated with diversity-productivity relationships in freshwater bacterial communities

Eukaryotic communities commonly display a positive relationship between biodiversity and ecosystem function (BEF) but the results have been mixed when assessed in bacterial communities. Habitat heterogeneity, a factor in eukaryotic BEFs, may explain these variable observations but it has not been thoroughly evaluated in bacterial communities. Here, we examined the impact of habitat on the relationship between diversity assessed based on the (phylogenetic) Hill diversity metrics and heterotrophic productivity. We sampled co-occurring free-living (more homogenous) and particle-associated (more heterogeneous) bacterial habitats in a freshwater, estuarine lake over three seasons: spring, summer and fall. There was a strong, positive, linear relationship between particle-associated bacterial richness and heterotrophic productivity that strengthened when considering dominant taxa. There were no observable BEF trends in free-living bacterial communities for any diversity metric. Biodiversity, richness and Inverse Simpson's index, were the best predictors of particle-associated production whereas pH was the best predictor of free-living production. Our findings show that heterotrophic productivity is positively correlated with the effective number of taxa and that BEF relationships are associated with microhabitats. These results add to the understanding of the highly distinct contributions to diversity and functioning contributed by bacteria in free-living and particle-associated habitats

Systematically Variable Planktonic Carbon Metabolism Along a Land-To-Lake Gradient in a Great Lakes Coastal Zone

During the summers of 2002–2013, we measured rates of carbon metabolism in surface waters of six sites across a land-to-lake gradient from the upstream end of drowned river-mouth Muskegon Lake (ML) (freshwater estuary) to 19 km offshore in Lake Michigan (LM) (a Great Lake). Despite considerable inter-year variability, the average rates of gross production (GP), respiration (R) and net production (NP) across ML (604 ± 58, 222 ± 22 and 381 ± 52 µg C L−1 day−1, respectively) decreased steeply in the furthest offshore LM site (22 ± 3, 55 ± 17 and −33 ± 15 µg C L−1day−1, respectively). Along this land-to-lake gradient, GP decreased by 96 ± 1%, whereas R only decreased by 75 ± 9%, variably influencing the carbon balance along this coastal zone. All ML sites were consistently net autotrophic (mean GP:R = 2.7), while the furthest offshore LM site was net heterotrophic (mean GP:R = 0.4). Our study suggests that pelagic waters of this Great Lakes coastal estuary are net carbon sinks that transition into net carbon sources offshore. Reactive and dynamic estuarine coastal zones everywhere may contribute similarly to regional and global carbon cycles

Chronicles of hypoxia: Time-series buoy observations reveal annually recurring seasonal basin-wide hypoxia in Muskegon Lake – A Great Lakes estuary

We chronicled the seasonally recurring hypolimnetic hypoxia in Muskegon Lake – a Great Lakes estuary over 3 years, and examined its causes and consequences. Muskegon Lake is a mesotrophic drowned river mouth that drains Michigan\u27s 2nd largest watershed into Lake Michigan. A buoy observatory tracked ecosystem changes in the Muskegon Lake Area of Concern (AOC), gathering vital time-series data on the lake\u27s water quality from early summer through late fall from 2011 to 2013 (www.gvsu.edu/buoy). Observatory-based measurements of dissolved oxygen (DO) tracked the gradual development, intensification and breakdown of hypoxia (mild hypoxia b4 mg DO/L, and severe hypoxia b2 mg DO/L) below the ~6 m thermocline in the lake, occurring in synchrony with changes in temperature and phytoplankton biomass in the water column during July–October. Time-series data suggest that proximal causes of the observed seasonal hypolimnetic DO dynamics are stratified summer water-column, reduced wind-driven mixing, longer summer residence time, episodic intrusions of cold DO-rich nearshore Lake Michigan water, nutrient run off from watershed, and phytoplankton blooms. Additional basin-wide water-column profiling (2011–2012) and ship-based seasonal surveys (2003–2013) confirmed that bottom water hypoxia is an annually recurring lake-wide condition. Volumetric hypolimnetic oxygen demand was high (0.07–0.15 mg DO/Liter/day) and comparable to other temperate eutrophic lakes. Over 3 years of intense monitoring, ~9–24% of Muskegon Lake\u27s volume experienced hypoxia for ~29–85 days/year – with the potential for hypolimnetic habitat degradation and sediment phosphorus release leading to further eutrophication. Thus, time-series observatories can provide penetrating insights into the inner workings of ecosystems and their external drivers