Bland J. Finlay

The Ubiquity of Small Species: Patterns of Local and Global Diversity

Abstract Small organisms (less than 1 millimeter in length) tend to have a cosmopolitan distribution. This is a consequence of huge absolute population sizes rather than any inherent properties of particular taxonomic groups. At the local scale, the diversity of small species exceeds that of larger organisms, but at the global scale this relation is reversed, because endemism is largely responsible for the species richness of large organisms. For small organisms, the relationship between species and area is flat, and a latitudinal diversity gradient is absent or weak. These patterns are explained by some of the assumptions underlying the unified neutral community model.

Ubiquitous dispersal of microbial species

The biosphere supports astronomical numbers of free-living microorganisms that belong to an indeterminate number of species. One view is that the abundance of microorganisms drives their dispersal, making them ubiquitous and resulting in a moderate global richness of species. But ubiquity is hard to demonstrate, not only because active species have a rapid turnover, but also because most species in a habitat at any moment in time are relatively rare or in some cryptic state. Here we use microbes that leave traces of their recent population growth in the form of siliceous scale structures to show that all species in the chrysomonad flagellate genus Paraphysomonas are probably ubiquitous.

Fluxes of methane and carbon dioxide from a small productive lake to the atmosphere

The fluxes of CH4 and CO2 to the atmosphere, and the relative contributions of ebullition and molecular diffusion, were determined for a small hypertrophic freshwater lake (Priest Pot, UK) over the period May to October 1997. The average total flux of CH4 and CO2 (estimated from 7 sites on the lake) was approximately 52 mmol m−2 d−1 and was apportioned 12 and 40 mmol m−2 d−1 toCH4 and CO2 respectively. Diffusion across the air-water interface accounted for the loss of 0.4and 40 mmol m−2 d−1 of CH4 and CO2 respectively whilst the corresponding figures for ebullition losses were 12.0 (CH4) and 0.23 (CO2) mmol m−2 d−1. Most CH4 (96%) was lost by ebullition, and most CO2 (99%) by diffusive processes. The ebullition of gas, measured at weekly intervals along a transect of the lake, showed high spatial and temporal variation. The CH4 content of the trapped gas varied between 44 and 88% (by volume) and was highest at the deepest points. Pulses of gas ebullition were detected during periods of rapidly falling barometric pressure. Therelevance of the measurements to global estimates ofcarbon emission from freshwaters are discussed.

Cosmopolitan Metapopulations of Free-Living Microbial Eukaryotes

Metapopulations of macroscopic organisms tend to be geographically restricted, but free-living protists and other microbial eukaryotes present a different picture. Here we show that most organisms smaller than 1 mm occur worldwide wherever their required habitats are realised. This is a consequence of ubiquitous dispersal driven by huge population sizes, and the consequently low probability of local extinction. Organisms larger than 10 mm are much less abundant, and rarely cosmopolitan. The supporting data, together with the discovery that the 1-10 mm size range accommodates a transition from cosmopolitan to regionally-restricted distribution, were derived from extensive inventories of eukaryotic species in a freshwater pond (1278 species), and a shallow marine bay (785 species). All accessible records were examined to establish the extent of global coverage by these species. Some groups of microbial eukaryotes are severely undersampled (e.g. naked amoebae; marine meiofauna in the southern hemisphere) but this fails to weaken evidence that metapopulations of microbial eukaryotes are cosmopolitan.

Local versus Global Diversity of Microorganisms: Cryptic Diversity of Ciliated Protozoa

Microbial species diversity. both global and local, is still poorly understood. In this study all species of ciliated protozoa were recorded microscopically from ∼1 cm 2 sediment collected from a small lake and from a marine shallow-water bay. Additional adjacent sediment samples (together representing <50 cm 2 ) then incubated under a variety of culture conditions to reveal cryptic species that are present as resting cysts or are too rare to be found microscopically. About 85 and of the total number of observed species from the limnic and marine sediment, respectively, were such cryptic species. In both cases the number of species found in < 50 cm 2 of sediment represented about 75% of all ciliate species ever recorded from these two previously well-studied habitats, and about 8% of all named free-living ciliates. These observations support the assumption that in the case of microorganisms everything is everywhere and that their global species diversity is relatively limited.

The use of rRNA sequences and fluorescent probes to investigate the phylogenetic positions of the anaerobic ciliate Metopus palaeformis and its archaeobacterial endosymbiont

The polymerase chain reaction (PCR) was used to amplify small-subunit ribosomal DNA from the anaerobic ciliated protozoon Metopus palaeformis, and from its uncultured endosymbiotic bacteria. This was accomplished directly from total DNA extracted from protozoa without prior isolation or enrichment for symbiont cells. The double-stranded amplification products were precipitated and directly sequenced using the linear PCR reaction. Fluorescent oligonucleotide probes were designed and used in whole-cell hybridizations to provide direct visual evidence that the sequences originated from the host ciliate and from the endosymbiont. Phylogenetic analysis of the Metopus palaeformis sequence consistently placed it as a deep-branching lineage near the root of the ciliate tree. However, the present data were insufficient to resolve the detailed relationship between Blepharisma and Metopus and thus to determine if the heterotrichs are mono- or paraphyletic. Phylogenetic analysis of the symbiont partial sequence clearly demonstrated that it is an archaeobacterium and that it is closely related to, but distinct from, Methanobacterium formicicum.

Multiple Origins of Anaerobic Ciliates with Hydrogenosomes within the Radiation of Aerobic Ciliates

Some ciliates live anaerobically and lack mitochondria, but possess hydrogenosomes: organelles that contain hydrogenase and produce hydrogen. The origin of hydrogenosomes has been explained by two competing hypotheses: (i) they are biochemically modified mitochondria; or (ii) they are derived from endosymbiotic association(s) of ciliates and anaerobic eubacteria that possessed the hydrogenosome biochemistry. Phylogenetic analyses of representative aerobic, and anaerobic hydrogenosomal ciliates using host nuclear SSU rDNA sequences indicate a minimum of three, but more likely four, separate origins of hydrogenosomes. Whereas this does not refute either hypothesis, the implausibility of multiple convergent endosymbioses gives further support to the view that hydrogenosomes in ciliates derive from an existing organelle, which ultrastructural evidence suggests is the mitochondrion. Our results indicate a considerable potential for physiological-biochemical plasticity among a group of predominantly aerobic eucaryotes, and provide a phylogenetic framework to further refine and test hypotheses of the origins of the hydrogenosomal enzymes.

Microbial diversity and activity in a Danish Fjord with anoxic deep water

Abstract Microbial diversity and activity were studied in a stratified basin of Mariager Fjord, Denmark in August 1994. The basin is about 30 m deep and the lower half of the water column is anoxic and sulphidic. The hydrographical and biological features of the system are described. Based on chemical gradient profiles and measurements of process rates, we found that the relative importance of sulphate reduction, denitrification and methanogenesis in terms of anaerobic terminal mineralisation was about 5:1:0.4. It is possible, however, that methanogenesis is underestimated because an unknown fraction of the methane production escaped by ebullition. It was estimated that 10–15 % of the net primary production is mineralised anaerobically. The mean residence time of methane, sulphide and ammonia beneath the chemocline is within the range 1.6–2.3 yrs. Chemolithotrophic production in the chemocline (sulphide oxidation and nitrification) accounted for about 3% of the net primary production of the system. Methan...

Hypothesis: The Rate and Scale of Dispersal of Freshwater Diatom Species is a Function of their Global Abundance

We have analysed the geographical records of a representative selection of extant diatom species from a freshwater pond. The more often a species is recorded in the ecological literature, the greater is its apparent global distribution. One explanation is that the frequently recorded species are globally abundant, whereas species that are infrequently recorded are globally rare. We suggest a model in which random dispersal is the dominant force driving large-scale distribution of species, with the rate and scale of dispersal largely determined by global population size. Thus species that are locally rare or abundant are likewise rare or abundant worldwide. It is predicted that many of the rarer diatom species will, with additional sampling effort, be shown to have wide geographical distribution, but this requires intensive studies focused on revealing species that are normally cryptic. The argument in favour of endemic diatom species is untenable, because it is not possible to disprove their existence elsewhere in the biosphere.

The biology of free-living anaerobic ciliates.

Anaerobic ciliates are incapable of using oxidative phosphorylation in their energy metabolism and they are more or less sensitive to oxygen. All anaerobic ciliates possess mitochondria-like organelles (with a double outer membrane and often a few cristae) but these do not contain typical mitochondrial enzymes (e.g., cytochromes, cytochrome oxidase). In some species these organelles are capable of fermenting pyruvate into acetate and H2 and they are then referred to as hydrogenosomes. At least six orders of ciliates include anaerobic species. It is concluded that the evolution of anaerobic forms has taken place independently within different taxonomic groups and that hydrogenosomes are modified mitochondria. Many anaerobic ciliates harbour ecto- or endosymbiotic bacteria. Several ciliate species which produce hydrogen as a metabolic waste product harbour endosymbiotic methanogenic bacteria; in some cases this symbiosis represents a mutualistic relationship in which the host controls the life cycle of the symbionts and gains from their presence in terms of growth rate and growth efficiency. Many marine anaerobic ciliates harbour ectosymbiotic bacteria, but the nature of these bacteria and the significance of the association is not yet understood. The present paper reviews what is known about the biology of anaerobic ciliates with special emphasis on free-living forms, including a discussion of their habitats and their role in the microbial communities of anoxic environments.