Laura A Katz

Smith College · Biological Sciences

Ciliates are single-celled microbial eukaryotes that diverged from other eukaryotic lineages over a billion years ago. The extensive evolutionary timespan of ciliate has led to enormous genetic and phenotypic changes, contributing significantly to their high level of diversity. Recent analyses based on molecular data have revealed numerous cases of...

In contrast to the canonical view that genomes cycle only between haploid and diploid states, many eukaryotes have dynamic genomes that change content throughout an individual’s life cycle. However, the few detailed studies of microeukaryotic life cycles render our understanding of eukaryotic genome dynamism incomplete. Foraminifera (Rhizaria) are...

The evolution of lineage-specific gene families remains poorly studied across the eukaryotic tree of life, with most analyses focusing on the recent evolution of de novo genes in model species. Here we explore the origins of lineage-specific genes in ciliates, a ~1 billion year old clade of microeukaryotes that are defined by their division of soma...

Knowledge of eukaryotic life cycles and associated genome dynamics stems largely from research on animals, plants, and a small number of “model” (i.e., easily cultivable) lineages. This skewed sampling results in an underappreciation of the variability among the many microeukaryotic lineages, which represent the bulk of eukaryotic biodiversity. The...

Many species of plants have evolved structures called phytotelmata that store water and trap detritus and prey. These structures house diverse communities of organisms, the inquiline microbiome, that aids breakdown of litter and prey. The invertebrate and bacterial food webs in these systems are well characterized, but less is known about microbial...

Advances in phylogenomics and high-throughput sequencing have allowed the reconstruction of deep phylogenetic relationships in the evolution of eukaryotes. Yet, the root of the eukaryotic tree of life remains elusive. The most popular hypothesis in textbooks and reviews is a root between Unikonta (Opisthokonta + Amoebozoa) and Bikonta (all other eu...

Vertical inheritance is foundational to Darwinian evolution, but fails to explain major innovations such as the rapid spread of antibiotic resistance among bacteria and the origin of photosynthesis in eukaryotes. While lateral gene transfer (LGT) is recognized as an evolutionary force in prokaryotes, the role of LGT in eukaryotic evolution is less...

The purpose of this study is to determine which taxonomic methods can elucidate clear and quantifiable differences between two cryptic ciliate species, and to test the utility of genome architecture as a new diagnostic character in the discrimination of otherwise indistinguishable taxa. Two cryptic tintinnid ciliates, Schmidingerella arcuata and Sc...

Foraminifera, classified in the supergroup Rhizaria, are a common and highly diverse group of mainly marine protists. Despite their evolutionary and ecological importance, only limited genomic data (one partial genome and nine transcriptomic datasets) have been published for this group. Foraminiferal molecular phylogeny is largely based on 18S rRNA...

Foraminifera include diverse shell‐building lineages found in a wide array of aquatic habitats from the deep‐sea to intertidal zones to brackish and freshwater ecosystems. Recent estimates of morphological and molecular foraminifera diversity have increased the knowledge of foraminiferal diversity, which is critical as these lineages are used as bi...

Ciliates are defined by the presence of dimorphic nuclei as they have both a somatic macronucleus and germline micronucleus within each individual cell. The size and structure of both germline micronuclei and somatic macronuclei varies tremendously among ciliates. Except just after conjugation (i.e. the nuclear exchange in sexual cycle), the germli...

Mobile genetic elements (MGEs) are transient genetic material that can move either within a single organism’s genome or between individuals or species. While historically considered ‘junk’ DNA (i.e. deleterious or at best neutral), more recent studies reveal the adaptive advantages MGEs provide in lineages across the tree of life. Ciliates, a group...

Though acting as a major component of eukaryotic biodiversity, many microbial eukaryotes remain poorly studied, including the focus of the present work, testate amoebae of the order Arcellinida (Amoebozoa) and non-model lineages of ciliates (Alveolata). In particular, knowledge of their genome structures and changes in genome content over their oft...

Microbial eukaryotes, i.e., protists, represent the bulk of eukaryotic diversity in terms of species diversity and biomass. Protists are globally distributed in all ecosystems and play important roles in food webs and nutrient cycles. To date it remains enigmatic how protist diversity is generated, especially in lineages with large populations in e...

Advances in phylogenetics and high-throughput sequencing have allowed the reconstruction of deep phylogenetic relationships in the evolution of eukaryotes. Yet, the root of the eukaryotic tree of life remains elusive. The most popular hypothesis in textbooks and reviews is a root between Unikonta (Opisthokonta + Amoebozoa) and Bikonta (all other eu...

Epigenetic processes in eukaryotes play important roles through regulation of gene expression, chromatin structure and genome rearrangements. Mechanisms such as chromatin modification (e.g. DNA methylation, histone modification) and non-protein-coding RNAs (npc-RNAs) have been well studied in animals and plants. With the exception of a few model or...

Schmidingerella arcuata is an ecologically important tintinnid ciliate that has long-served as a model species in plankton trophic ecology. We present a partial micronuclear genome and macronuclear transcriptome resource for S. arcuata, acquired using single-cell techniques, and we report on pilot analyses including functional annotation and genome...

Testate (shell‐building) amoebae, such as the Arcellinida (Amoebozoa), are useful bioindicators for climate change. Though past work has relied on morphological analyses to characterize Arcellinida diversity, genetic analyses revealed the presence of multiple cryptic species underlying morphospecies. Here, we design and deploy Arcellinida‐specific...

While nuclear small subunit ribosomal DNA (nSSU rDNA) is the most commonly-used gene marker in studying phylogeny, ecology, abundance, and biodiversity of microbial eukaryotes, mitochondrial small subunit ribosomal DNA (mtSSU rDNA) provides an alternative. Recently, both copy number variation and sequence variation of nSSU rDNA have been demonstrat...

Arcella, a diverse understudied genus of testate amoebae is a member of Tubulinea in Amoebozoa group. Transcriptomes are a powerful tool for characterization of these organisms as they are an efficient way of characterizing the protein‐coding potential of the genome. In this work, we employed both single‐cell and clonal populations transcriptomics...

The availability of high-throughput sequencing (HTS) has transformed our understanding of the diversity of microbial eukaryotes (i.e., protists) across diverse habitats. Yet relating this biodiversity to function remains a challenge, particularly in the context of microbial food webs. Here we perform a set of microcosm experiments to evaluate the i...

Ciliates, a eukaryotic clade that is over 1 billion years old, are defined by division of genome function between transcriptionally inactive germline micronuclei and functional somatic macronuclei. To date, most analyses of gene family evolution have been limited to cultivable model lineages (e.g., Tetrahymena , Paramecium , Oxytricha , and Stylony...

Testate amoebae (Amoebozoa, Arcellinida) are a group of unicellular eukaryotes that build shells around their cell. These shells are well preserved in the fossil record. Arcellinida communities are sensitive to environmental changes, such as shifts in temperature, moisture and pH. Therefore, they have been used extensively as bioindicators to recon...

Shell-building amoebae (Amoebozoa) are microbial eukaryotes that are highly abundant in freshwater ecosystems and represent top predators (i.e. feed on other microbes, small animals). Because of their abundance, sensitivity to abiotic environmental factors and the preservation of their tests in the fossil record, testate amoebae serve as excellent...

Estimating multiple sequence alignments (MSAs) and inferring phylogenies are essential for many aspects of comparative biology. Yet, many bioinformatics tools for such analyses have focused on specific clades, with greatest attention paid to plants, animals and fungi. The rapid increase of high-throughput sequencing (HTS) data from diverse lineages...

We used an experimental approach of analyzing marine microcosms to evaluate the impact of both predation (top-down) and food resources (bottom-up) on spirotrich ciliate communities. To assess the diversity, we used two molecular methods-denaturing gradient gel electrophoresis (DGGE) and high-throughput sequencing (HTS). We carried out two types of...

As a model organism for studies of cell and environmental biology, the free-living and cosmopolitan ciliate Euplotes vannus shows intriguing features like dual genome architecture (i.e. separate germline and somatic nuclei in each cell/organism), "gene-sized" chromosomes, stop codon reassignment, programmed ribosomal frameshifting (PRF) and strong...

Sequence-based approaches, such as analyses of ribosome DNA (rDNA) clone libraries and high-throughput amplicon sequencing, have been used extensively to infer evolutionary relationships and elucidate the biodiversity in microbial communities. However, recent studies demonstrate both rDNA copy number variation and intra-individual (intra-genomic) s...

The emergence of robust single-cell 'omics techniques enables studies of uncultivable species, allowing for the (re)discovery of diverse genomic features. In this study, we combine single-cell genomics and transcriptomics to explore genome evolution in ciliates, a > 1 billion year old clade. Analysis of the data resulting from these single-cell 'om...

Despite their diversity and ecological importance, many areas of the SAR—Stramenopila, Alveolata, and Rhizaria—clade are poorly understood as the majority (90%) of SAR species lack molecular data and only 5% of species are from well-sampled families. Here, we review and summarize the state of knowledge about the three major clades of SAR, describin...

The genome of P. falciparum, the causative agent of malaria in Africa, has been extensively studied since it was first fully sequenced in 2002. However, many open questions remain, including understanding the chromosomal context of molecular evolutionary changes (e.g. relationship between chromosome map and phylogenetic conservation, patterns of ge...

Separate germline and somatic genomes are found in numerous lineages across the eukaryotic tree of life, often separated into distinct tissues (e.g., in plants, animals, and fungi) or distinct nuclei sharing a common cytoplasm (e.g., in ciliates and some foraminifera). In ciliates, germline-limited (i.e., micronuclear-specific) DNA is eliminated du...

Genome structure and nuclear organization have been intensely studied in model ciliates such as Tetrahymena and Paramecium, yet few studies have focused on nuclear features of other ciliate clades including the class Karyorelictea. In most ciliates, both the somatic macronuclei and germline micronuclei divide during cell division and macronuclear d...

Blepharisma americanum, a member of the understudied ciliate class Heterotrichea, has a moniliform somatic macronucleus that resembles beads on a string. B. americanum is distinguishable by its pink coloration derived from the autofluorescent pigment blepharismin and tends to have a single somatic macronucleus with 3-6 nodes and multiple germline m...

Sex is beneficial in eukaryotes as it can increase genetic diversity, reshuffle their genomes, and purge deleterious mutations. Yet, its evolution remains a mystery. The eukaryotic clade supergroup Amoebozoa encompasses diverse lineages of polymorphic amoeboid forms, including both free-living and parasitic lineages. The group is generally believed...

Although protists (microbial eukaryotes) provide an important link between bacteria and Metazoa in food webs, we do not yet have a clear understanding of the spatial scales on which protist diversity varies. Here, we use a combination of DNA fingerprinting (denaturant gradient gel electrophoresis or DGGE) and high-throughput sequencing (HTS) to ass...

Analyses of estimated diversity from inshore to offshore and by depth reveal no clear pattern and few differences between nanosize (2–10μm) and microsize (10–80μm). A total of 100 (11±8 for nanosize and microsize) and 500 reads (20±13 and 24±16 OTUs for the nanosize and microsize, respectively) was subsampled for A and B, respectively. The diversit...

Ciliate communities composition (percentage of reads) for abundant OTUs (more than 5% of the total number of reads) at 99% ID shows constancy in pattern within the offshore stations compared to the midshelf and inshore stations. In contrast, there is evidence of a bloom at all depths in two non-adjacent inshore samples (i.e. stations 34 and 36). Ea...

Phylogenetic tree shows the similarity between OTUs obtained by DGGE and HTS. In black, HTS OTUs with more than 1,000 reads were considered to simplify the tree. In orange are the OTUs from DGGE analyses (See Fig 3). OTU with an asterisk were not represented in Fig 4. (DOCX)

Principal coordinate analyses using Fast Unifrac dissimilarity metric do not show clear clustering of Ciliates community composition at small scale (1, 2, and 3 km) for the offshore and midshelf. (DOCX)

Pearson correlations show complex relationship between OTUs and environmental parameters. Some abundant OTUs are related to the distance to the shore and to the depth (e.g. OTU329 mainly observed inshore or OTU2594 mainly observed within the surface layers in the offshore location) as observed in Fig 4. (DOCX)

Canonical correlation analysis shows only that salinity and temperature are major abiotic features across sites. (DOCX)

Reads, OTU numbers (with or without subsampling) and diversity indices (See S1 Fig). (DOCX)

Venn diagrams show specificity of OTUs for a size, a position on the shore and/or for a layer, but also the presence of a core community (23 OTUs) in all our samples. (DOCX)

OTU best BLAST results to a morphospecies (see S2 Fig). (DOCX)

Marine microbial eukaryotes play critical roles in planktonic food webs and have been described as most diverse in the photic zone where productivity is high. We used high-throughput sequencing (HTS) to analyze the spatial distribution of planktonic ciliate diversity from shallow waters (<30m depth) to beyond the continental shelf (>800m depth) alo...

A sequestered germline in Metazoa has been argued to be an obstacle to lateral gene transfer (LGT), though few studies have specifically assessed this claim. Here we test the hypothesis that the origin of a sequestered germline reduced LGT events in Bilateria (i.e. triploblast lineages) as compared to early-diverging Metazoa (i.e. Ctenophora, Cnida...

The relationship between nuclear architecture and patterns of molecular evolution in lineages across the eukaryotic tree of life is not well understood, partly because molecular evolution is traditionally explored as changes in base pairs along a linear sequence without considering the context of nuclear position of chromosomes. The ciliate Chilodo...

Our knowledge on microbial biogeography depends on the way we define and study diversity. In contrast to most microbes, some protist lineages have conspicuous structures that allow comparisons of diversity concepts and measures—those based on molecules and those based on morphology. We analyzed a group of shell-bearing planktonic ciliates, the tint...

Genome architecture varies considerably among eukaryotes in terms of both size and structure (e.g. distribution of sequences within the genome, elimination of DNA during formation of somatic nuclei). The diversity in eukaryotic genome architectures and the dynamic processes are only possible due to the well-developed epigenetic toolkit, which proba...

This study reveals extensive phenotypic convergence based on the non-monophyly of genera and morphospecies of testate (shelled) amoebae. Using two independent markers, small subunit ribosomal DNA (ssu-rDNA) and mitochondrial cytochrome oxidase I (COI), we demonstrate discordance between morphology and molecules for 'core Nebela' species (Arcellinid...

While there is compelling evidence for the impact of endosymbiotic gene transfer (EGT; transfer from either mitochondrion or chloroplast to the nucleus) on genome evolution in eukaryotes, the role of interdomain transfer from bacteria and/or archaea (i.e. prokaryotes) is less clear. Lateral gene transfers (LGTs) have been argued to be potential sou...

Significance Scientists have used gene sequences and morphological data to construct tens of thousands of evolutionary trees that describe the evolutionary history of animals, plants, and microbes. This study is the first, to our knowledge, to apply an efficient and automated process for assembling published trees into a complete tree of life. This...

Reconstructing the phylogenetic relationships that unite all lineages (the tree of life) is a grand challenge. The paucity of homologous character data across disparately related lineages currently renders direct phylogenetic inference untenable. To reconstruct a comprehensive tree of life we therefore synthesized published phylogenies, together wi...

Microbes are critical members of marine ecosystems, given their roles as both primary producers and consumers in food webs. Despite their importance, data on biogeographical patterns of microbial eukaryotes are limited. Past studies have generally targeted either all eukaryotes or broad clades like Rhizaria and Alveolata. For this study, we focus m...

ABSTRACT Chromosome rearrangements occur in a variety of eukaryotic life cycles, including during the development of the somatic macronuclear genome in ciliates. Previous work on the phyllopharyngean ciliate Chilodonella uncinata revealed that macronuclear β-tubulin and protein kinase gene families share alternatively processed germ line segments...

Most eukaryotic lineages are microbial, and many have only recently been sampled for phylogenetic studies or remain in the "dark area" of the tree of life where there are no molecular data. To assess relationships among eukaryotic lineages, we perform a taxon-rich phylogenomic analysis including 232 eukaryotes selected to maximize taxonomic diversi...

The isolate ATCC® 50979™ is a small amoebozoan whose actin gene was previously characterized, but did not allow a stable phylogenetic placement. This isolate was originally mis-identified upon deposition, and subsequently mis-illustrated in a recent publication. Here, we provide both a detailed morphological description as well as additional molecu...

Microscopy has revealed tremendous diversity of bacterial and eukaryotic forms. Recent molecular analyses show discor-dance in estimates of biodiversity between morphological and molecular analyses. Moreover, phylogenetic analyses of the diversity of microbial forms reveal evidence of convergence at scales as deep as interdomain: morphologies share...

Lateral gene transfer (LGT) has impacted the evolutionary history of eukaryotes, though to a lesser extent than in bacteria and archaea. Detecting LGT and distinguishing it from single gene tree artifacts is difficult, particularly when considering very ancient events (i.e., over hundreds of millions of years). Here, we use two independent lines of...

In some ciliates, extensive genome fragmentation leads to a macronucleus (i.e. somatic nucleus) containing gene-sized chromosomes that vary in copy number. Yet the relationship between copy number and expression level is not well understood as previous work has shown a variety of patterns. For example, nanochromosome copy numbers are positively cor...

Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the world's oceans.

Cyclidiids and thigmotrichids are two diverse groups of scuticociliates, a diverse clade of ciliates that is often difficult to investigate due to the small size and conserved morphology among its members. Compared to other groups (e.g. hypotrichs and oligotrichs), the scuticociliates have received relatively little attention and their phylogenetic...

Recent advances such as high-throughput sequencing (HTS) have changed conceptions about the magnitude of diversity on Earth. This is especially true for microbial lineages, which have seen the discovery of great numbers of rare forms in places such as the human gut as well as diverse environments (e.g., freshwater, marine, and soil). Given the diff...

Background Understanding the evolutionary relationships of all eukaryotes on Earth remains a paramount goal of modern biology, yet analyzing homologous sequences across 1.8 billion years of eukaryotic evolution is challenging. Many existing tools for identifying gene orthologs are inadequate when working with heterogeneous rates of evolution and en...

In most lineages, diversity among gene family members results from gene duplication followed by sequence divergence. Because of the genome rearrangements during the development of somatic nuclei, gene family evolution in ciliates involves more complex processes. Previous work on the ciliate Chilodonella uncinata revealed that macronuclear β-tubulin...

Only a limited number of studies exist on the life cycles of non-model ciliates such as Chilodonella uncinata (Cl: Phyllopharyngea). The handful of papers on this taxon indicates the presence of a heteromeric macronucleus, marked by separate DNA rich and DNA poor regions. Here, we study the life cycle of C. uncinata using confocal laser scanning mi...

Genomes are dynamic in lineages across the tree of life. Among bacteria and archaea, for example, DNA content varies throughout life cycles and non-binary cell division in diverse lineages indicates the need for coordination of the inheritance of genomes. These observations contrast with the textbook view that bacterial and archaeal genomes are mon...

We assessed the diversity of coastal planktonic ciliates (Oligotrichia and Choreotrichia, Class: Spirotrichea) in Fishers Island Sound off the coast of Connecticut, USA using a combination of denaturant gradient gel electrophoresis (DGGE) and morphological analyses. To test the hypothesis that ciliate communities followed water masses, we sampled 3...

Assessing microbial diversity requires analysis of all three domains of life, including eukaryotic microbes. We examined the diversity of two ecologically important clades of microbial eukaryotes, ciliates in the subclasses Oligotrichia and Choreotrichia (class Spirotrichea), by comparing pyrosequencing to Sanger-sequenced clone libraries and micro...

Mitochondrial SSU-rDNA has been used recently to infer phylogenetic relationships among a few ciliates. Here, this locus is compared with nuclear SSU-rDNA for uncovering the deepest nodes in the ciliate tree of life using broad taxon sampling. Nuclear and mitochondrial SSU-rDNA reveal the same relationships for nodes well-supported in previously-pu...

List of 74 specialized journals surveyed for seed plant phylogenies. (DOC)

Corresponding author's response to emails (2) requesting alignments and trees from previously published study. Number in parenthesis subtending organismal group represents number of authors contacted. (DOCX)

Description of methods used for this study. (DOC)

Quality survey from 344 publications that did have data publicly available on TreeBASE (see Text S1). (TIF)

List of specialized journals (see definition in Text S1) examined here. (DOCX)

List of nonspecialized, broad audience journals (see definition in Text S1) examined here. (DOC)

Failure to archive published data can impede reproducibility and inhibit downstream synthesis. Alarmingly, we estimate that ∼70% of existing DNA sequence alignments/phylogenetic trees, representing much of the underpinning of modern phylogenetic analysis, are no longer accessible. The evolutionary biology community needs to adopt policies ensuring...

Cytochrome B sequences and allozymes reveal complex patterns of molecular variation in dusky salamander (Desmognathus) populations in eastern Tennessee. One group of allozymically distinctive populations, which we refer to as the Sinking Creek form (SCF), combines morphological attributes of Desmognathus fuscus with cytB sequences characteristic of...