Insights into the Biogeographical Patterns of Planktonic Diatom Diversity

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Habitats and adaptations

As prolific phototrophic organisms, diatoms can live in the open ocean, polar waters, tropical waters, all fresh water areas, soil, snow and even glacial ice. During the course of evolution they have developed different adaptations to survive within each environment. The two main adaptations are (i) storing energy as oils that allow them to be suspended in the water column, and (ii) strong silica frustules that protect them from predation. Additionally, planktonic species often have morphological adaptations that allow them to remain suspended in water. These adaptations to prevent sinking include forming long chains, linked by silica spines (Gersonade and Harwood, 1990). This type of linkage is the most common mode of chain formation and has been seen in radial centric diatoms such as Paralia, Stephanopyxix and Aulacosiera, in the multipolar centrics Detonula and Skeletonema, in araphid pennates Staurosira, Fragilarioforma and Fragilaria, and even in raphid pennates such as Diadesmis (Falkowski and Knoll, 2011). Other diatom species grow attached to surfaces like rocks or aquatic plants, e.g. Licmorphora and Tabularia. Their frustules are shaped in such a way to aid in attachment. Some species form short stalks, or mucilage pads, while others form long branching stalks, that hold the cells in place and are resistant to waves or high flow in rivers. Apical pads often lead to characteristic zig-zag or stellate (star-shaped) colonies, that resist sinking, found in many araphid pennates and bipolar centrics (Falkowski and Knoll, 2011). Diatoms that have a raphe system (Figure 1.2) are able to move over benthic surfaces, whether the surfaces are fine grains of sand, or within the mud of a tidal zone, or even on other diatoms. A few diatoms also form mucilage tubes and move up and down inside the tubes (Figure 1.4).

Life history

Diatoms are able to reproduce both sexually and asexually, but primarily by a unique “shrinking division” mode of asexual reproduction (Figure 1.5A). During cell division, the two valves get separated, each of them forming the epivalve of the daughter cells and new hypovalves are secreted
within the parent cell (Figure 1.3). As the rigid, siliceous cell walls of silica cannot expand, the daughter cells get gradually smaller and smaller. This decrease in cell size with each successive vegetative division continues until it is within a range where environmental parameters may induce sexual reproduction (Edlund and Stoemer, 1997). Gamete formation occurs and they fuse to form a zygote which then gives rise to an auxospore (Figure 1.5B). An auxospore possesses a lightly silicified cell wall (perizonia), which allows the cell to expand to its maximum size and then produces a frustule with the normal cell morphology (Kaczmarska et al., 2000, 2011; Wehr and Sheath, 2003). Hence, in diatoms, sexual reproduction is not only a means of inducing genetic variability but also facilitates the enlargement of cells back to their maximum size. In response to stress, i.e. in conditions of low nutrient supply or poor sunlight, diatom cells may form metabolically inactive spores called resting spores (Horner, 2002). Following the onset of favorable conditions, the cells may regain normal functioning.

Secondary endosymbiosis

Diatoms have a complex evolutionary origin and, hence, their genome is called a ‘mix-and-match genome’ (Armbrust, 2009). Their genomes are the product of a secondary endosymbiosis event in which a heterotrophic eukaryote engulfed a photoautotrophic one and, instead of digesting it, shared with it the ability of photosynthesize (Delwiche, 1999; Bhattacharya and Medlin, 1995). This event led to six different classes of organisms within the Chromalveolate grouping (which incorporates both the Straemnopiles and Alveolates (Fig. 1.1A); Cavalier-Smith, 1999), i.e. Haptophytes, Cryptomonads, Stramenopiles, Ciliates, Apicomplexa, Dinoflagellates (Figure 1.6A). This was a sequential event, initially a eukaryotic heterotroph engulfed a cyanobacterium to form the photosynthetic plastids of the Plantae (land plants and red and green algae) (Figure 1.6B; Yoon, 2004). This resulted in wholesale gene transfer from the symbiotic cyanobacterial genome to the host nucleus (Reyes-Prieto, 2006).
This primary endosymbiosis was followed by a secondary endosymbiosis event where a different eukaryotic heterotroph captured a red alga (Figure 1.6C). Gene transfer continued from the red-algal nuclear and plastid genomes to the host nucleus (Armbrust, 2004). Nosenko and Bhattacharya (2007) identified genes of green algal origin in chromalveolates. This finding led to a hypothesis that they might have originated from an ancient green algal endosymbiont. Later, Moustafa et al. (2009) found the evidence of hundreds of genes of green algal origin in diatoms, supporting the hypothesis that a green alga was involved during the secondary endosymbiosis. Bowler et al. (2008) reported at least 170 red algal genes in the nuclear genome of diatoms, most of which seem to encode plastid components. Owing to this evolutionary history, diatom plastids have been reported to carry out various processes that are characteristic of Plantae plastids, like, photosynthesis, biosynthesis of fatty acids, isoprenoids and amino acids (Armbrust, 2009, Qui et al., 2013). Apart from these, the aforementioned union has sanctified them with a distinctive range of attributes. The most significant is the presence of a urea cycle, which was thought to be restricted to animals (Armbrust, 2004).
It can be speculated that diatoms have a potentially advantageous range of abilities that would not normally be found in a single organism. The silica frustule, thought to be inherited from the exosymbiont, aids in protection from predation, pathogens and desiccation, as well as focusing light into the cell (refs). The subsequent gains (and losses) of specific genes, largely from bacteria, presumably helped them adapt to new ecological niches (Armbrust, 2009). Overall, these processes and many others derived from this unique evolutionary background have ensured their success, making them a highly adaptable group of species with several advantages over other phytoplankton.

Evolutionary and geological history

Fossil records. According to (incomplete) fossil records, the emergence of diatoms took place in the Triassic period (250 Myr ago), although the earliest well-preserved diatom fossils come from the Early Jurassic era (190 Myr ago) (Sorhannus, 2007, Sims, 2006, Armbrust, 2009). The most definitive fossil records for centric diatoms came from the Cretaceous (~145 Myr ago) with the earliest fossil records of araphid (lacking a raphe) pennate diatoms dating from the Late Cretaceous (~145 Myr ago), and raphid pennates from the Middle Eocene (~56.5 Myr ago) (Figure 1.7). The earliest freshwater diatoms appeared in the Palaeocene (~65 Myr ago) in Russia and the Late Eocene (~56.5 Myr ago) in North America. However, there are reports of Precambrian (~570 Myr ago) and Triassic (~245 Myr ago) fossils that might be diatoms or diatom relatives (Sims et al., 2006). This belief on diatoms having earlier evolutionary history than expected comes from the property of the silica that it recrystallizes under pressure, which in turn, can destroy diatom fossils. Through the ages, diatom frustules settled down to the bottom of lakes or oceans forming thick deposits of diatomite, or diatomaceous earth. These appear as deposits of white chalky material and are the richest sources of diatom fossils (Benten and Harper, 2013). Diatomaceous earth has a range of commercial applications (see Section 1.1.7).
The rise of diatoms. Following mass extinction in the Cretaceous (~ 65 Myr ago), almost 85% of life was lost, leading to extensive reductions in marine diversity. However, diatoms managed to survive and began to colonize offshore areas, including the open ocean (Armbrust, 2009). Rabosky and Sorhannus (2009) reported that diatom diversity was highest at the Eocene/Oligocene boundary (~30 Myr ago). This era also saw the emergence of raphid pennates, which brought the ability to glide along surfaces and hence expanded the ecological niches greatly (Armbrust, 2009).

Diatom classification

Morphotaxonomy. Diatoms have been classified in different ways by different authors. Round et al. (1990) classified diatoms as a division (Bacillariophyta), whereas Van den Hoek et al. (1995) considered diatoms as a class (Bacillariophyceae or Diatomophyceae) within the division Heterokontophyta. Historically, taxonomists have divided diatoms into two or three major groups, based primarily on the organization of the pattern of striae on the valve. Round et al. (1990) divided the diatoms into three classes: Coscinodiscophyceae, Fragilariophyceae and Bacillariophyceae, which corresponded to three of the main types of valve organization. Informally, these three structural variants can be referred to as ‘centrics’ (Coscinodiscophyceae), ‘araphid pennates’ (Fragilariophyceae) and ‘raphid pennates’ (Bacillariophyceae). Van den Hoek et al. (1995) proposed two major groups of diatoms, Centrales and Pennales. Coscinodiscophyceae and the Centrales are more or less synonymous and are more informally known as the “centric” diatoms. Fragilariophyceae and Bacillariophyceae together correspond to the Pennales and comprise the so-called “pennate” diatoms (Figure 1.8).
Molecular phylogeny. In more recent years, molecular markers such as genomic DNA fragments, have been used for phylogenetic analyses to elucidate the evolutionary history of living organisms (Zagoskin et al., 2007). These conserved DNA or RNA nucleotide sequences have enabled researchers, on the one hand, to solve phylogenies at higher taxonomic levels and, on the other, to resolve highly variable sequences to dissect affinities at the species level. One such widely used example of DNA region for reconstructing phylogenies are the genes encoding the ribosomal RNA subunits (rDNAs). The rDNAs encode the RNA components of the ribosome (rRNAs) and form two subunits, the large subunit (LSU) and small subunit (SSU). In most eukaryotes, the 18S rRNA is the small ribosomal subunit, and the large subunit contains three rRNA species (the 5S, 5.8S and 28S rRNAs in mammals, and the 25S rRNA in plants). The rRNA-encoding genes are typically organized in clusters and are separated by internal transcribed spacers (ITS1 and ITS2) and an intergenic spacer (Figure 1.9A; Gerbi, 1985).
Owing to the presence of rRNA-encoding rDNAs in all living organisms, rDNA sequences have become a popular choice for molecular taxonomy as it is possible to construct phylogenies for all taxa. The phylogenetic power of rDNA has been repeatedly demonstrated in a wide range of organisms from animals (Freeland and Boag, 1999), including humans (Gonzalez et al., 1990), to higher plants (Alvarez and Wendel, 2003), protists (Sim et al., 2006; Hoshina et al., 2006; Johnson et al., 2007), and fungi (Lutzoni ety al., 2001). Most of the 18S rDNA (region encoding the 18S rRNA) is highly conserved and is generally used for phylogenetic studies at higher taxonomic levels. The tertiary structure of the small subunit ribosomal RNA (SSU rRNA) has been resolved by X-ray crystallography (Yusupov, 2001). The secondary structure of SSU rRNA contains 4 distinct domains — the 5′, central, 3′ major, and 3′ minor domains (Figure 1.9B).
Kooistra et al. (2003) used 38 diatom SSU sequences and showed “raphid pennates in a well-supported clade within a paraphyletic araphid group. The pennates as a whole were monophyletic within an apparently paraphyletic group of multipolar centric diatoms. The latter group was essentially composed of a series of clades that collapsed in a polytomy because their basal dichotomies remained unsupported. Pennates and multipolar centrics formed a weakly supported clade, which was sister to radial centrics”.
Based on molecular and morphological data, Medlin & Kaczmarska (2004) proposed a replacement for the traditional view suggesting two new subdivisions (Coscinodiscophytina and Bacillariophytina) for diatoms and a new class, the Mediophyceae, for the bipolar centrics. Adl et al. (2005) adopted Medlin & Kaczmarska’s names but treated both the Coscinodiscophyceae and Mediophyceae as paraphyletic taxa (groups that do not include all of the descendents of a single common ancestor).
Theriot et al (2009) proposed a diatom phylogeny based on the nuclear-encoded small subunit of the 18S rDNA gene (SSU) which weakly rejected the classification given by Medlin & Kaczmarska (2004) and others (Sims et al., 2006; Medlin et al. (2008) using parsimony analysis and morphological data. Their results showed that only the Bacillariophyceae (pennate diatoms) were monophyletic, in contrast to Medlin & Kaczmarska (2004) and Sims et al. (2006) who proposed monophyly for each of the Coscinodiscophyceae, Mediophyceae, and Bacillariophyceae.
The diatom phylogeny inferred from 18S rDNA-gene regions of diatoms, shown in Figure 1.10, reveals a principal dichotomy leading to a clade of radial centrics (basal clade) and another with multipolar centrics and pennates. The latter exhibited polytomy (a node which has more than two immediate descending branches) containing several clades. The multipolar centrics clade, characterized by a bi-, tri- or multipolar symmetry, cluster in two main polytomic clades. They have been shown to share certain features with araphid pennates, for instance, the ability to produce mucilage from the valve apical pore. They can inhabit both benthic and planktonic environments. Diatoms belonging to the araphid pennate clade constitute a paraphyletic group (i.e. group that does not include all of the descendents of a single common ancestor) consisting of 5 main polytomic clades. Like multipolar centric diatoms, araphid diatoms display a wide range of shapes and life-styles. They are characterized by elongated valves and the ability to form colonies. They can also have both benthic and planktonic lifestyles. Raphid pennates are the only monophyletic group (i.e. each member is a descendent of a single common ancestor) consisting of cells equipped with the raphe slit. This organelle allows raphid pennates to slide on a substrate and thus, this group abounds in benthic environments. However, many have been reported to have gone back to their planktonic life-styles. In conclusion, it seems that the raphids evolved from araphids and that araphids in their turn are derived from centrics. A similar scenario is supported by the sexual reproduction patterns in these groups, with the evolutionary trend moving from oogamy (ancestral state in centrics) to anisogamy (in pennates) passing through isogamy and imperfect isogamy.

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Global importance

Owing to their physiology, diatoms exhibit a remarkable impact on various global phenomena. Their photosynthesis, biogenic silica formation, environmental diversity and a tendency to dominate phytoplankton communities, have led to the major involvement of diatoms in primary production, nutrient cycling, the biological carbon pump, and at the base of the food chain. It has been estimated that diatoms contribute 40–45% oceanic primary productivity, which amounts to 20% of global carbon fixation and oxygen production (Yool and Tyrrell, 2003). Due to the presence of the silica frustule, they play an important role in the biological carbon pump because they facilitate the sinking of organic matter below the photic zone to the ocean floor which provides both essential nutrients for organisms living in the ocean depths and export of carbon to the ocean interior. This makes them a key player in the biological pump as well as the silica cycle.
Diatom growth is limited by factors such as nutrient availability; however, when there are large nutrient influxes or seasonal changes, diatoms can form large blooms up to several square kilometers in size. When the nutrients, principally nitrate and silicate, get depleted, the bloom dissipates, forming aggregates of silicified cells that sink to the ocean floor. This accumulation of diatom frustules in sediment forms diatomaceous earth, a material that is used in a number of industrial applications such as abrasive pastes, water filters, fillers, insulators, and (non-toxic) insecticides (Mann, 1917). Furthermore, most petroleum deposits are derived from diatoms that have sedimented to the seafloor over geochemical time scales (Denman, 2008). The structural and physical properties of the frustule are the focus of several research areas into nanotechnological applications. These include drug delivery solar technology, microfluidics, catalyst production and bio-sensing. Lipid production in diatoms is also drawing interest as a source of renewable oil. Although the global contributions made by diatoms are already significant, these technologies may be the key to drawing the public eye to the importance of these microscopic algae and the roles they play for the well-being of our planet.

Table of contents :

1. Diatom Biodiversity Assessment: General Introduction
1.1. Diatoms: life in glass houses
1.1.1. Diatom ultrastructure
1.1.2. Habitats and adaptations
1.1.3. Life history
1.1.4. Secondary endosymbiosis
1.1.5. Evolutionary and geological history
1.1.6. Diatom classification
1.1.7. Global importance
1.2. Marine biodiversity and biogeography
1.2.1. General introduction
1.2.2. Characterizing biodiversity
1.2.3. Microbial biogeography: processes and patterns in microbial diversity
1.2.4. Future directions in the study of microbial biogeography
1.3. Metabarcoding: a new paradigm for biodiversity assessment
1.4. Tara Oceans: a comprehensive sampling of marine planktonic biota
1.4.1. Background
1.4.2. Sampling strategy and methodology
1.4.3. Tara Oceans integrated pipeline
1.5. Aim of the thesis
1.6. Thesis outline
2. Insights into the Biogeographical Patterns of Planktonic Diatom Diversity – an Assessment Using Metabarcoding
2.1. Introduction
2.2. Results
2.2.1. Evaluation of V9 region of 18S rDNA as a diversity marker for diatoms
2.2.2. Global dataset of diatom V9 metabarcodes
2.2.3. Diatom community composition
2.2.4. Unassigned sequences/ Novelty
2.2.5. Comparison between light microscopy and V9 ribotype counts
2.2.6. Global diversity patterns
2.2.7. Community similarity
2.3. Discussion
2.4. Materials and methods
2.4.1. Distance based Analysis
2.3.2. Metabarcoding dataset
2.3.3. Morphological analyses
2.3.4. Taxonomy-based clustering
2.3.5. Global distribution analysis
Figure legends
Supplementary Material
3. Niche-based and Spatial Processes Shaping Diatom Community Structure
3.1. Introduction
3.2. Materials and methods
3.2.1. Dataset
3.2.2. Statistical analyses
3.3. Results
3.3.1. Distance-decay relationships (DDR)
3.3.2. Mantel analysis
3.3.3. Multiple regression analyses on individual environmental variables
3.3.4. Relative role of niche-based and spatial processes
3.4. Discussion
4. A Metabarcoding-based Assessment of Diatom Assemblages
4.1. Introduction
4.2. Materials and methods
4.2.1. Study area and dataset
4.2.2. Statistical analyses
4.3. Results
4.3.1. Ordination of environmental variables
4.3.2. Correlation of individual variables to each ribotype
4.3.3. Taxonomic and environmental characterization
4.3.4. Spatial characterization at local scale
4.3.5. Spatial characterization at regional scale
4.3.6. Environmental determinants of the global distribution of clusters
4.4. Discussion
5. Discerning and Quantifying Power-law Behavior of Protistan Communities
5.1. Introduction
5.1.1. Marine community structure: evident structuring processes
5.1.2. Overview on rank-abundance distribution (RAD) curve
5.1.3. Commonness and rarity
5.1.4. Power-law distribution
5.1.5. Structure of the study
5.2. Materials and methods
5.2.1. Protist dataset
5.2.2. Delineating rare ribotypes in the world’s ocean
5.2.3. Fitting power-laws to the community data
5.3. Results
5.3.1. Potential insights into commonness and rarity patterns of protists
5.3.2. Discerning, quantifying and comparing power-law behavior
5.4. Discussion
5.4.1. Potential insights into commonness and rarity patterns in the world’s ocean
5.4.2. How plankton gets dispersed in random environment
5.4.3. Power laws in ecology
5.4.4. Explanations of power-laws
6. General Conclusion and Future Perspectives
A. Glossary
B. Diversity and similarity Indices
C. Multivariate statistical methods
D. Resolution of V9 18S rDNA tags in diatom phylogeny
E. Supplementary Information to Chapter 2
F. Supplementary Information to Chapter 3
G. Supplementary Information to Chapter 4
H. Supplementary Information to Chapter 5
I. Co-authored manuscripts


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