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1. Genome Streamlining, Proteorhodopsin, and Organic Nitrogen Metabolism in Freshwater Nitrifiers

   https://doi.org/10.1128/mbio.02379-21  

   Podowski, Justin C.; Paver, Sara F.; Newton, Ryan J.; Coleman, Maureen L. (June 2022, mBio)

   Giovannoni, Stephen J. (Ed.)

   ABSTRACT Microbial nitrification is a critical process governing nitrogen availability in aquatic systems. Freshwater nitrifiers have received little attention, leaving many unanswered questions about their taxonomic distribution, functional potential, and ecological interactions. Here, we reconstructed genomes to infer the metabolism and ecology of free-living picoplanktonic nitrifiers across the Laurentian Great Lakes, a connected series of five of Earth’s largest lakes. Surprisingly, ammonia-oxidizing bacteria (AOB) related to Nitrosospira dominated over ammonia-oxidizing archaea (AOA) at nearly all stations, with distinct ecotypes prevailing in the transparent, oligotrophic upper lakes compared to Lakes Erie and Ontario. Unexpectedly, one ecotype of Nitrosospira encodes proteorhodopsin, which could enhance survival under conditions where ammonia oxidation is inhibited or substrate limited. Nitrite-oxidizing bacteria (NOB) “ Candidatus Nitrotoga” and Nitrospira fluctuated in dominance, with the latter prevailing in deeper, less-productive basins. Genome reconstructions reveal highly reduced genomes and features consistent with genome streamlining, along with diverse adaptations to sunlight and oxidative stress and widespread capacity for organic nitrogen use. Our findings expand the known functional diversity of nitrifiers and establish their ecological genomics in large lake ecosystems. By elucidating links between microbial biodiversity and biogeochemical cycling, our work also informs ecosystem models of the Laurentian Great Lakes, a critical freshwater resource experiencing rapid environmental change. IMPORTANCE Microorganisms play critical roles in Earth’s nitrogen cycle. In lakes, microorganisms called nitrifiers derive energy from reduced nitrogen compounds. In doing so, they transform nitrogen into a form that can ultimately be lost to the atmosphere by a process called denitrification, which helps mitigate nitrogen pollution from fertilizer runoff and sewage. Despite their importance, freshwater nitrifiers are virtually unexplored. To understand their diversity and function, we reconstructed genomes of freshwater nitrifiers across some of Earth’s largest freshwater lakes, the Laurentian Great Lakes. We discovered several new species of nitrifiers specialized for clear low-nutrient waters and distinct species in comparatively turbid Lake Erie. Surprisingly, one species may be able to harness light energy by using a protein called proteorhodopsin, despite the fact that nitrifiers typically live in deep dark water. Our work reveals the unique biodiversity of the Great Lakes and fills key gaps in our knowledge of an important microbial group, the nitrifiers. 

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2. Coexisting picoplankton experience different relative grazing pressures across an ocean productivity gradient

   https://doi.org/10.1073/pnas.2220771120  

   Landry, Michael R.; Stukel, Michael R.; Selph, Karen E.; Goericke, Ralf (October 2023, Proceedings of the National Academy of Sciences)

   Picophytoplankton populations [Prochlorococcus,Synechococcus(SYN), and picoeukaryotes] are dominant primary producers in the open ocean and projected to become more important with climate change. Their fates can vary, however, with microbial food web complexities. In the California Current Ecosystem, picophytoplankton biomass and abundance peak in waters of intermediate productivity and decrease at higher production. Using experimental data from eight cruises crossing the pronounced CCE trophic gradient, we tested the hypothesis that these declines are driven by intensified grazing on heterotrophic bacteria (HBAC) passed to similarly sized picophytoplankton via shared predators. Results confirm previously observed distributions as well as significant increases in bacterial abundance, cell growth, and grazing mortality with primary production. Mortalities of picophytoplankton, however, diverge from the bacterial mortality trend such that relative grazing rates on SYN compared to HBAC decline by 12-fold between low and high productivity waters. The large shifts in mortality rate ratios for coexisting populations are not explained by size variability but rather suggest high selectivity of grazer assemblages or tightly coupled tradeoffs in microbial growth advantages and grazing vulnerabilities. These findings challenge the long-held view that protistan grazing mainly determines overall biomass of microbial communities while viruses uniquely regulate diversity by “killing the winners”. 

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3. RAD‐tag and mitochondrial DNA sequencing reveal the genetic structure of a widespread and regionally imperiled freshwater mussel, Obovaria olivaria (Bivalvia: Unionidae)

   https://doi.org/10.1002/ece3.8560  

   Bucholz, Jamie R.; Sard, Nicholas M.; VanTassel, Nichelle M.; Lozier, Jeffrey D.; Morris, Todd J.; Paquet, Annie; Zanatta, David T. (January 2022, Ecology and Evolution)

   Abstract Obovaria olivariais a species of freshwater mussel native to the Mississippi River and Laurentian Great Lakes‐St. Lawrence River drainages of North America. This mussel has experienced population declines across large parts of its distribution and is imperiled in many jurisdictions.Obovaria olivariauses the similarly imperiledAcipenser fulvescens(Lake Sturgeon) as a host for its glochidia. We employed mitochondrial DNA sequencing and restriction site‐associated DNA sequencing (RAD‐seq) to assess patterns of genetic diversity and population structure ofO. olivariafrom 19 collection locations including the St. Lawrence River drainage, the Great Lakes drainage, the Upper Mississippi River drainage, the Ohioan River drainage, and the Mississippi Embayment. Heterozygosity was highest in Upper Mississippi and Great Lakes populations, followed by a reduction in diversity and relative effective population size in the St. Lawrence populations. PairwiseF_STranged from 0.00 to 0.20, and analyses of genetic structure revealed two major ancestral populations, one including all St. Lawrence River/Ottawa River sites and the other including remaining sites; however, significant admixture and isolation by river distance across the range were evident. The genetic diversity and structure ofO. olivariais consistent with the existing literature onAcipenser fulvescensand suggests that, although northern and southernO. olivariapopulations are genetically distinct, genetic structure inO. olivariais largely clinal rather than discrete across its range. Conservation and restoration efforts ofO. olivariashould prioritize the maintenance and restoration of locations whereO. olivariaremain, especially in northern rivers, and to ensure connectivity that will facilitate dispersal ofAcipenser fulvescensand movement of encysted glochidia. 

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4. A century of intermittent eco‐evolutionary feedbacks resulted in novel trait combinations in invasive Great Lakes alewives ( Alosa pseudoharengus )

   https://doi.org/10.1111/eva.13063  

   Smith, Shelby E.; Palkovacs, Eric P.; Weidel, Brian C.; Bunnell, David B.; Jones, Andrew W.; Bloom, Devin D. (August 2020, Evolutionary Applications)

   Abstract Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco‐evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large‐bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non‐native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present‐day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long‐distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations. 

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5. Investigating the morphological and genetic divergence of arctic char ( Salvelinus alpinus) populations in lakes of arctic Alaska

   https://doi.org/10.1002/ece3.7211  

   Klobucar, Stephen_L; Rick, Jessica_A; Mandeville, Elizabeth_G; Wagner, Catherine_E; Budy, Phaedra (March 2021, Ecology and Evolution)

   Abstract Polymorphism facilitates coexistence of divergent morphs (e.g., phenotypes) of the same species by minimizing intraspecific competition, especially when resources are limiting. Arctic char (Salvelinussp.) are a Holarctic fish often forming morphologically, and sometimes genetically, divergent morphs. In this study, we assessed the morphological and genetic diversity and divergence of 263 individuals from seven populations of arctic char with varying length‐frequency distributions across two distinct groups of lakes in northern Alaska. Despite close geographic proximity, each lake group occurs on landscapes with different glacial ages and surface water connectivity, and thus was likely colonized by fishes at different times. Across lakes, a continuum of physical (e.g., lake area, maximum depth) and biological characteristics (e.g., primary productivity, fish density) exists, likely contributing to characteristics of present‐day char populations. Although some lakes exhibit bimodal size distributions, using model‐based clustering of morphometric traits corrected for allometry, we did not detect morphological differences within and across char populations. Genomic analyses using 15,934 SNPs obtained from genotyping by sequencing demonstrated differences among lake groups related to historical biogeography, but within lake groups and within individual lakes, genetic differentiation was not related to total body length. We used PERMANOVA to identify environmental and biological factors related to observed char size structure. Significant predictors included water transparency (i.e., a primary productivity proxy), char density (fish·ha^‐1), and lake group. Larger char occurred in lakes with greater primary production and lower char densities, suggesting less intraspecific competition and resource limitation. Thus, char populations in more productive and connected lakes may prove more stable to environmental changes, relative to food‐limited and closed lakes, if lake productivity increases concomitantly. Our findings provide some of the first descriptions of genomic characteristics of char populations in arctic Alaska, and offer important consideration for the persistence of these populations for subsistence and conservation. 

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