Papers by Bopaiah Biddanda
bioRxiv (Cold Spring Harbor Laboratory), Dec 11, 2017
Eukaryotic communities commonly display a positive relationship between biodiversity and ecosyste... more Eukaryotic communities commonly display a positive relationship between biodiversity and ecosystem function (BEF). Based on current studies, it remains uncertain to what extent these findings extend to bacterial communities. An extrapolation from eukaryotic relationships would predict there to be no BEF relationships for bacterial communities because they are generally composed of an order of magnitude more taxa than the communities in most eukaryotic BEF studies. Here, we sampled surface water of a freshwater, estuarine lake to evaluate BEF relationships in bacterial communities across a natural productivity gradient. We assessed the impact of habitat heterogeneity-an important factor influencing eukaryotic BEFs-on the relationship between species richness, evenness, phylogenetic diversity, and heterotrophic productivity by sampling co-occurring free-living (more homogenous) and particle-associated (more heterogeneous) bacterial habitats. Diversity measures, and not environmental variables, were the best predictors of particles-associated heterotrophic production. There was a strong, positive, linear relationship between particle-associated bacterial richness and heterotrophic productivity that was strengthened when considering evenness. There were no observable BEF trends in free-living bacterial communities. In contrast, per-capita but not community-wide heterotrophic productivity increased across both habitats as communities were composed of taxa that were more phylogenetically clustered. This association indicates that communities with more phylogenetically related taxa have higher per-capita heterotrophic production than communities of phylogenetically distantly related taxa. Our findings show that lake heterotrophic bacterial productivity can be positively affected by evenness and richness, negatively by phylogenetic diversity, and that BEF relationships are contingent on microhabitats. These results .
MSystems, Oct 29, 2019
High-nucleic-acid (HNA) and low-nucleic-acid (LNA) bacteria are two operational groups identified... more 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 ϭ 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.
Biogeochemistry, Dec 1, 2016
Many lacustrine systems, despite management efforts to control eutrophication, are hypoxic during... more Many lacustrine systems, despite management efforts to control eutrophication, are hypoxic during stratified periods. Hypoxia is a major concern, not only for its impact on aquatic life but also for its potential to stimulate production of the greenhouse gases, methane (CH 4) and nitrous oxide (N 2 O). We investigated the drivers of hypoxia in Muskegon Lake, a temperate dimictic freshwater estuary that experiences frequent hypolimnetic mixing due to atmospheric forces, riverine inputs, and intrusion of oxic water from coastal upwelling in Lake Michigan. Primary production and respiration (R) rates obtained from a d 18 O mass balance model were similar to other mesotrophic environments (0.56-26.31 and 0.57-13.15 mmol O 2 m-3 day-1 , respectively), although high P/R (C2 in midsummer) indicated there is sufficient autochthonous production to support hypoxia development and persistence. The isotopic enrichment factor for respiration (e obs) varied markedly and was least negative in August of both sampling years, consistent with high R rates. Hypoxic conditions were associated with accumulation of N 2 O but not CH 4 , and emissions of N 2 O are among the highest reported from lakes. The average N 2 O site preference value of 25.4% indicates that the majority of N 2 O was produced by nitrification via hydroxylamine oxidation, despite the presence of resilient hypoxia. While it has been hypothesized that denitrification acts as a sink for N 2 O in hypoxic lakes, it is clear that Muskegon Lake functions as a strong source of N 2 O via nitrification. Further considerations of lakes as global sources of N 2 O thus warrant a closer evaluation of nitrification-fueled N 2 O production.
Ecosystems, Jun 8, 2017
The occurrence of bottom-water hypoxia is increasing in bodies of water around the world. Hypoxia... more The occurrence of bottom-water hypoxia is increasing in bodies of water around the world. Hypoxia is of concern due to the way it negatively impacts lakes and estuaries at the whole ecosystem level. During 2015, we examined the influence of hypoxia on the Muskegon Lake ecosystem by collecting surface-and bottom-water nutrient samples, bacterial abundance counts, benthic fish community information, and performing profiles of chlorophyll and phycocyanin as proxies for phytoplankton and cyanobacterial growth, respectively. Several significant changes occurred in the bottom waters of the Muskegon Lake ecosystem as a result of hypoxia. Lake-wide concentrations of soluble reactive phosphorus (SRP) and total phosphorus increased with decreasing dissolved oxygen (DO). Bacterial abundance was significantly lower when DO was less than 2.2 mg L-1. Whereas there were no drastic changes in surface chlorophyll a concentration through the season, phycocyanin increased threefold during and following a series of major wind-mixing events. Phycocyanin remained elevated for over 1.5 months despite several strong wind events, suggesting that high SRP concentrations in the bottom waters may have mixed into the surface waters, sustaining the bloom. The fish assemblage in the hypolimnion also changed in association with hypoxia. Overall fish abundance, number of species, and maximum length all decreased in catch as a function of bottom DO concentrations. The link between hypoxia and wind events appears to serve as a positive feedback loop by continuing internal loading and cyanobacterial blooms in the lake, while simultaneously eroding habitat quality for benthic fish.
Journal of Great Lakes Research, Dec 1, 2019
Hypoxia formation and breakdown were tracked during 2015 in Muskegon Lake estuary at multiple loc... more Hypoxia formation and breakdown were tracked during 2015 in Muskegon Lake estuary at multiple locations, and five years (2011-2015) of time-series buoy observatory data were evaluated for the effect of episodic wind-events on lake mixing. Biweekly water temperature and dissolved oxygen (DO) profiles at four locations revealed that hypoxia occurred at all sites and persisted for 2-3 months during summer 2015. On one date in late-summer, up to 24% of the lake's volume was estimated to be mildly hypoxic (DO < 4 mg L À1) as defined by lake sturgeon requirements. Patterns of wind speed and water column stability in late spring indicated that high winds and low stability delayed the onset of hypoxia while in late summer low winds and high stability delayed degradation of hypoxia. Wind speeds appear to play a great role in the interannual variability of stratification and subsequent hypoxia. Water temperature and DO profiles taken before and after one midsummer mixing event (wind speed >7.7 m s À1 for 10 h), indicated that while the wind was unable to completely mix the entire water column, it deepened the epilimnion by $1.5 m and sheared a thin layer from the upper hypolimnion. By entraining internally loaded nutrients, such episodic wind-events may initiate and sustain algal blooms in nutrient limited surface waters. Quantifying the variable role of wind and mixing events will be key to integrating limnological processes into climate models of the future.
Journal of Great Lakes Research, Feb 1, 2023
Animal migrations mark the largest daily movement of biomass on Earth today, but who performed th... more Animal migrations mark the largest daily movement of biomass on Earth today, but who performed the first diurnal migration? Extant benthic microbial mats inhabiting Lake Huro's low-oxygen, high-sul...
Journal of Great Lakes Research, Jul 1, 2023
Hydrobiology, Jun 17, 2023
Marine Ecology, Sep 1, 1992
Journal of Phycology, May 5, 2023
Cyanobacteria are diverse prokaryotic, photosynthetic organisms present in nearly every known eco... more Cyanobacteria are diverse prokaryotic, photosynthetic organisms present in nearly every known ecosystem. Recent investigations around the world have recovered vast amounts of novel biodiversity in seldom sampled habitats. One phylogenetically significant character, the secondary folding structures of the 16S–23S ITS rDNA region, has allowed an unprecedented capacity to erect new species. However, two questions arise: Is this feature as informative as is proposed, and how do we best employ these features? Submerged sinkholes with oxygen‐poor, sulfur‐rich ground water in Lake Huron (USA) contain microbial mats dominated by both oxygenic and anoxygenic cyanobacteria. We sought to document some of this unique cyanobacterial diversity. Using culture‐based investigations, we recovered 45 strains, of which 23 were analyzed employing 16S–23S rDNA sequences, ITS folding patterns, ecology, and morphology. With scant morphological discontinuities and nebulous 16S rDNA gene sequence divergence, ITS folding patterns were effective at articulating cryptic biodiversity. However, we would have missed these features had we not folded all the available motifs from the strains, including those with highly similar 16S rDNA gene sequences. If we had relied solely on morphological or 16S rDNA gene data, then we might well have missed the diversity of Anagnostidinema. Thus, in order to avoid conformation basis, which is potentially common when employing ITS structures, we advocate clustering strains based on ITS rDNA region patterns independently and comparing them back to 16S rDNA gene phylogenies. Using a total evidence approach, we erected a new taxon according to the International Code of Nomenclature for Algae, Fungi, and Plants: Anagnostidinema visiae.
Freshwater Science, Aug 17, 2021
Around the world, freshwater lakes are increasingly suffering from harmful algal blooms (HABs) as... more Around the world, freshwater lakes are increasingly suffering from harmful algal blooms (HABs) as a result of anthropogenic eutrophication. Muskegon Lake (Muskegon, Michigan, USA), a drowned river mouth, Great Lakes estuary, was declared an Area of Concern by the Environmental Protection Agency in 1987 with nuisance algal blooms cited as a beneficial-use impairment. The objective of this study was to quantify changes in HAB prevalence and assemblage composition in Muskegon Lake over 14 y (2003–2016) and explore the environmental factors potentially driving the changes. We performed univariate and multivariate analyses on long-term monitoring data, including environmental and phytoplankton data, to understand their relationships and temporal variation. Using linear regressions, we assessed changes in environmental variables over time and relationships between cyanobacteria biovolume and environmental variables. We used non-metric multidimensional scaling to visualize variation in annual cyanobacteria assemblage composition and association with environmental variables. Analyses revealed that, despite generally rising water temperatures, which would be expected to increase HABs, a reduction in nutrient concentrations caused by restoration efforts has likely led to substantial decreases in HAB abundance over time. Additionally, HAB assemblage composition appears to be driven by temperature and nutrient form and amount, with Microcystis (Lemmermann, 1907) often dominating. HABs in freshwater bodies should be closely monitored into the future as we enter an era of uncertain climatic conditions.
American Geophysical Union eBooks, Feb 1, 2016
Abstracts with programs, 2018
Journal of Great Lakes Research, 2015
of the Biddanda lab for their extensive help in field collections and laboratory assistance on th... more of the Biddanda lab for their extensive help in field collections and laboratory assistance on this research project. Thank you to Brian Scull, of the Rediske Lab, for running the nutrient assays which were crucial to describing the land-to-lake gradient. Thanks to Sandra McLellan at UW-Milwaukee for support during manuscript preparation.
Frontiers in Microbiology, May 8, 2017
Little is known about large sulfur bacteria (LSB) that inhabit sulfidic groundwater seeps in larg... more Little is known about large sulfur bacteria (LSB) that inhabit sulfidic groundwater seeps in large lakes. To examine how geochemically relevant microbial metabolisms are partitioned among community members, we conducted metagenomic analysis of a chemosynthetic microbial mat in the Isolated Sinkhole, which is in a deep, aphotic environment of Lake Huron. For comparison, we also analyzed a white mat in an artesian fountain that is fed by groundwater similar to Isolated Sinkhole, but that sits in shallow water and is exposed to sunlight. De novo assembly and binning of metagenomic data from these two communities yielded near complete genomes and revealed representatives of two families of LSB. The Isolated Sinkhole community was dominated by novel members of the Beggiatoaceae that are phylogenetically intermediate between known freshwater and marine groups. Several of these Beggiatoaceae had 16S rRNA genes that contained introns previously observed only in marine taxa. The Alpena fountain was dominated by populations closely related to Thiothrix lacustris and an SM1 euryarchaeon known to live symbiotically with Thiothrix spp. The SM1 genomic bin contained evidence of H 2-based lithoautotrophy. Genomic bins of both the Thiothrix and Beggiatoaceae contained genes for sulfur oxidation via the rDsr pathway, H 2 oxidation via Ni-Fe hydrogenases, and the use of O 2 and nitrate as electron acceptors. Mats at both sites also contained Deltaproteobacteria with genes for dissimilatory sulfate reduction (sat, apr, and dsr) and hydrogen oxidation (Ni-Fe hydrogenases). Overall, the microbial mats at the two sites held low-diversity microbial communities, displayed evidence of coupled sulfur cycling, and did not differ largely in their metabolic potentials, despite the environmental differences. These results show that groundwaterfed communities in an artesian fountain and in submerged sinkholes of Lake Huron are a rich source of novel LSB, associated heterotrophic and sulfate-reducing bacteria, and archaea.
Geological Society of America Abstracts with Programs, 2020
Aquatic Biology, Mar 3, 2011
Groundwater can be an important source of nutrients and energy to aquatic ecosystems, but quantif... more Groundwater can be an important source of nutrients and energy to aquatic ecosystems, but quantifying the inputs and biogeochemical importance remains challenging. A series of submerged groundwater vents in northern Lake Huron were examined to determine the linkage between groundwater nutrients and aquatic food webs. We collected samples of key food-web components from groundwater vent and reference habitats and analyzed them for 13 C, 15 N, and 34 S isotopes. Dissolved inorganic carbon (DIC) in the groundwater was depleted in 13 C, while aqueous sulfate was enriched in 34 S (mean differences between groundwater and reference sites were-3.9 ‰ and +12.0 ‰, respectively). Benthic primary producers, macroinvertebrates, and benthivorous fish had significantly lower δ 13 C values in groundwater environments, and benthivorous fish were somewhat depleted (-2.5 ‰) in δ 34 S at groundwater sites compared to reference sites. However, δ 15 N values were not different between groundwater and reference sites, and pelagic components of the ecosystems (plankton and planktivorous and piscivorous fish) were similar in both δ 13 C and δ 15 N. These data suggest benthic metazoan communities surrounding groundwater vents are partially linked to groundwater-derived benthic primary production, while planktivorous and piscivorous communities not directly associated with the benthos do not rely on groundwater nutrients. KEY WORDS: Stable isotopes • Submerged sinkholes • Groundwater • Food web • Lake Huron Resale or republication not permitted without written consent of the publisher Underwater image showing purple cyanobacterial benthic mats thriving in a 2 m layer of dense sulfur-rich groundwater in Middle Island Sinkhole, Lake Huron (Inset, aerial photo of 100 m sinkhole with 7 m boat) Photos: Rob Paddock, Scott Kendall (inset)
AGU Fall Meeting Abstracts, Dec 1, 2013
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Papers by Bopaiah Biddanda