Division of labor and recurrent evolution of polymorphisms in a group of colonial animals

Rendering developmental and ecological processes into macroevolutionary events and trends has proved to be a difficult undertaking, not least because processes and outcomes occur at different scales. Here we attempt to integrate comparative analyses that bear on this problem, drawing from a system that has seldom been used in this way: the co-occurrence of alternate phenotypes within genetic individuals, and repeated evolution of distinct categories of these phenotypes. In cheilostome bryozoans, zooid polymorphs (avicularia) and some skeletal structures (several frontal shield types and brood chambers) that evolved from polymorphs have arisen convergently at different times in evolutionary history, apparently reflecting evolvability inherent in modular organization of their colonial bodies. We suggest that division of labor evident in the morphology and functional capacity of polymorphs and other structural modules likely evolved, at least in part, in response to the persistent, diffuse selective influence of predation by small motile invertebrate epibionts.     

The evolutionary history of division of labour

Functional specialization, or division of labour (DOL), of parts within organisms and colonies is common in most multi-cellular, colonial and social organisms, but it is far from ubiquitous. Several mechanisms have been proposed to explain the evolutionary origins of DOL; the basic feature common to all of them is that functional differences can arise easily. These mechanisms cannot explain the many groups of colonial and social animals that exhibit no DOL despite up to 500 million years of evolution. Here, I propose a new hypothesis, based on a multi-level selection theory, which predicts that a reproductive DOL is required to evolve prior to subsequent functional specialization. I test this hypothesis using a dataset consisting of the type of DOL for living and extinct colonial and social animals. The frequency distribution of DOL and the sequence of its acquisition confirm that reproductive specialization evolves prior to functional specialization. A corollary of this hypothesis is observed in colonial, social and also within multi-cellular organisms; those species without a reproductive DOL have a smaller range of internal variation, in terms of the number of polymorphs or cell types, than species with a reproductive DOL.     

Life in the colonies: learning the alien ways of colonial organisms

Who needs to go to outer space to study alien beings when the oceans of our own planet abound with bizarre and unknown creatures? Many of them belong to sessile clonal and colonial groups, including sponges, hydroids, corals, octocorals, ascidians, bryozoans, and some polychaetes. Their life histories, in many ways unlike our own, are a challenge for biologists. Studying their ecology, behavior, and taxonomy means trying to “think like a colony” to understand the factors important in their lives. Until the 1980s, most marine ecologists ignored these difficult modular organisms. Plant ecologists showed them ways to deal with the two levels of asexually produced modules and genetic individuals, leading to a surge in research on the ecology of clonal and colonial marine invertebrates. Bryozoans make excellent model colonial animals. Their life histories range from ephemeral to perennial. Aspects of their lives such as growth, reproduction, partial mortality due to predation or fouling, and the behavior of both autozooids and polymorphs can be studied at the level of the colony, as well as that of the individual module, in living colonies and over time.     

The evolutionary transition to coloniality promotes higher blood parasitism in birds

Parasitism has been argued as one of the major costs of breeding sociality in birds. However, there is no clear evidence for an increased parasite pressure associated with the evolutionary transition from solitary to colonial breeding. I used the pairwise comparative method to test whether colonial bird species incur in a greater risk of infection and if they must to face with a greater diversity of blood parasites (Haematozoa), by comparing pairs of congeners that included one solitary and one colonial breeding species. The richness, both in terms of number of species and number of genera, as well as the prevalence of blood parasites resulted higher in colonial species than in their solitary breeding sisters, while controlling for differences in research effort and other potentially confounding effects. These results point towards higher transmission rates of blood parasites among colonial hosts. Given the detrimental effects of blood parasites on their host fitness, the higher risk of infection and the exposition to a more diverse parasite fauna may have imposed an important cost associated to the evolution of avian coloniality. This may help to explain why colonial species have larger immune system organs, as well as to explore differences in other host life history traits potentially shaped by blood parasites.     

The development and evolution of hydrozoan polyp and colony form

Hydrozoans represent an extremely diverse group of mostly colonial forms. Despite this tremendous diversity, many of the morphological differences between hydrozoan species can be attributed to simple changes in the relative position of regions/structures along the axes of the polyp and the stolon or hydrocaulus from which polyps bud. Many genes have been implicated in the specification of positional information along the axis of the polyp. Knowledge from these studies in Hydra, and from comparative studies in Hydractinia polyp polymorphs, suggests that evolutionary changes in the regulation of axial patterning genes may be a prominent mechanism underlying hydrozoan evolution. Despite the paucity of interspecies comparative expression information, hypotheses can be formulated about the role of developmental regulatory genes in hydrozoan evolution from information available from Hydra.     

Coupling astogenic aging in the colonial tunicate Botryllus schlosseri with the stress protein mortalin

Botryllus schlosseri, a colonial marine invertebrate, exhibits three generations of short-lived astogenic modules that continuously grow and die throughout the colony's entire lifespan, within week-long repeating budding cycles (blastogenesis), each consisting of four stages (A-D). At stage D, aging is followed by the complete absorption of adult modules (zooids) via a massive apoptotic process. Here we studied in Botryllus the protein mortalin (HSP70s member), a molecule largely known for its association with aging and proliferation. In-situ hybridization and qPCR assays reveal that mortalin follows the cyclic pattern of blastogenesis. Colonies at blastogenic stage D display the highest mortalin levels, and young modules exhibit elevated mortalin levels compared to old modules. Manipulations of mortalin with the specific allosteric inhibitor MKT-077 has led to a decrease in the modules’ growth rate and the development of abnormal somatic/germinal morphologies (primarily in vasculature and in organs such as the endostyle, the stomach and gonads). We therefore propose that mortalin plays a significant role in the astogeny and aging of colonial modules in B. schlosseri, by direct involvement in the regulation of blastogenesis.     

Increased inter-colony fusion rates are associated with reduced COI haplotype diversity in an invasive colonial ascidian Didemnum vexillum

Considerable progress in our understanding of the population genetic changes associated with biological invasions has been made over the past decade. Using selectively neutral loci, it has been established that reductions in genetic diversity, reflecting founder effects, have occurred during the establishment of some invasive populations. However, some colonial organisms may actually gain an ecological advantage from reduced genetic diversity because of the associated reduction in inter-colony conflict. Here we report population genetic analyses, along with colony fusion experiments, for a highly invasive colonial ascidian, Didemnum vexillum. Analyses based on mitochondrial cytochrome oxidase I (COI) partial coding sequences revealed two distinct D. vexillum clades. One COI clade appears to be restricted to the probable native region (i.e., north-west Pacific Ocean), while the other clade is present in widely dispersed temperate coastal waters around the world. This clade structure was supported by 18S ribosomal DNA (rDNA) sequence data, which revealed a one base-pair difference between the two clades. Recently established populations of D. vexillum in New Zealand displayed greatly reduced COI genetic diversity when compared with D. vexillum in Japan. In association with this reduction in genetic diversity was a significantly higher inter-colony fusion rate between randomly paired New Zealand D. vexillum colonies (80%, standard deviation ±18%) when compared with colonies found in Japan (27%, standard deviation ±15%). The results of this study add to growing evidence that for colonial organisms reductions in population level genetic diversity may alter colony interaction dynamics and enhance the invasive potential of newly colonizing species.     

Investigation of bacteria with polyketide synthase genes and antimicrobial activity isolated from South China Sea sponges

Aims:  To obtain bacteria with PKS (polyketide synthase) genes and antimicrobial activity from sponges.
Methods and Results:  Eighteen bacteria with KS (ketosynthase) genes were identified by polymerase chain reaction (PCR) screening of 98 isolates from South China Sea sponges, Stelletta tenuis , Halichondria rugosa , Dysidea avara and Craniella australiensis . 16S rRNA gene-based B last analysis indicated that 15 isolates belonged to the phylum Firmicutes , among which 14 isolates were closely related to genus Bacillus , and 1 to Staphylococcus lentus . Two isolates were identified as actinomycetes, and one as Alcaligenes sp. in the phylum Proteobacteria . The 18 KS domains belong to trans-AT type I PKS and match PKS of marine bacterial symbionts. The 18 bacteria exhibited broad-spectrum antimicrobial activities against fungi, gram-positive and gram-negative bacteria. A 21·8-kb PKS gene cluster fragment containing five modules was isolated from the Staphylococcus lentus isolate A75 by screening of a fosmid library.
Conclusions:  The PKS gene diversity and different antimicrobial spectra indicate the potential of bacteria associated with South China Sea sponges for diverse polyketide production.
Significance and Impact of the Study:  Combined with bioactivity assay the PKS gene-based approach can be applied to efficient screening of strains of pharmaceutical value and the prediction of related compounds.     

A phylogenomic framework for charting the diversity and evolution of giant viruses

Large DNA viruses of the phylum Nucleocytoviricota have recently emerged as important members of ecosystems around the globe that challenge traditional views of viral complexity. Numerous members of this phylum that cannot be classified within established families have recently been reported, and there is presently a strong need for a robust phylogenomic and taxonomic framework for these viruses. Here, we report a comprehensive phylogenomic analysis of the Nucleocytoviricota, present a set of giant virus orthologous groups (GVOGs) together with a benchmarked reference phylogeny, and delineate a hierarchical taxonomy within this phylum. We show that the majority of Nucleocytoviricota diversity can be partitioned into 6 orders, 32 families, and 344 genera, substantially expanding the number of currently recognized taxonomic ranks for these viruses. We integrate our results within a taxonomy that has been adopted for all viruses to establish a unifying framework for the study of Nucleocytoviricota diversity, evolution, and environmental distribution.

Giant viruses have transformed our understanding of viral complexity, but we lack a framework for examining their diversity in the biosphere. This study presents a phylogenomic resource for charting the diversity, ecology, and evolution of giant viruses.     

Bio-prospecting Bacterial Diversity of Hot Springs in Northern Himalayan Region of India for Laccases

Bacterial diversity of hot springs of northern Himalayan region of India was studied and explored for laccases, the multicopper enzymes applicable in a large number of industries due to their ability to utilize a wide range of substrates. 220 operational taxonomic units (OTUs) out of 5551 sequence reads for bacterial diversity and 3 OTUs out of 19 sequence reads for Laccase like multicopper oxidases (LMCOs) diversity were generated. Bacteroidetes (74.28%) was the most abundant phylum including genus Paludibacter (66.96%), followed by phylum Proteobacteria (24.53%) including genera Chitinilyticum (7.55%) and Cellvibrio (6.14%). In case of laccase diversity, three LMCO sequences showed affiliation with proteobacteria and one with two domain laccase from uncultivable bacteroidetes. LMCO sequences belonged to H and N families.     

Contribution of the Actinobacteria to the growing diversity of lantibiotics

Currently, 76 lantibiotics have been described; the vast majority being produced by members of the Firmicute phylum of bacteria. There is a growing number being identified from the Actinobacteria phylum and some of these exhibit novel modifications leading to an increased functional diversity among lantibiotics. In this review, we discuss the currently characterized lantibiotics highlighting the expanding diversity provided by those from the Actinobacteria. This increased diversity has the potential to expand lantibiotic applications as antimicrobials in foods and pharmaceuticals. In addition, a phylogenetic classification system based on the full prepropeptide sequences showed remarkable consistency with current classification systems and may provide a more rapid and convenient means for classifying lantibiotics.     

Phylogenetic diversity of microorganisms associated with the deep-water sponge Baikalospongia intermedia

The diversity of bacteria associated with deep-water sponge Baikalospongia intermedia was evaluated by sequence analysis of 16S rRNA genes from two sponge samples collected in Lake Baikal from depths of 550 and 1204 m. A total of 64 operational taxonomic units, belonging to nine bacterial phyla, Proteobacteria (classes Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria), Actinobacteria, Planctomycetes, Cloroflexi, Verrucomicrobia, Acidobacteria, Chlorobi, and Nitrospirae, including candidate phylum WS5, were identified. Phylogenetic analysis showed that the examined communities contained phylotypes exhibiting homology to uncultured bacteria from different lake ecosystems, freshwater sediments, soil and geological formations. Moreover, a number of phylotypes were relative to psychrophilic, methane-oxidizing, sulfate-reducing bacteria, and to microorganisms resistant to the influence of heavy metals. It is noted that the unusual habitation conditions of deep-water sponges contribute to the taxonomic diversity of associated bacteria and have an influence on the presence of functionally important microorganisms in bacterial communities.     

Detection and Phylogenetic Relationships of Highly Diverse Uncultured Acidobacterial Communities in Altamira Cave Using 23S rRNA Sequence Analyses

Acidobacteria have been established as a novel and widespread bacterial phylum consistently detected during 16S rDNA-based molecular surveys. Recently, representatives of the phylum Acidobacteria were found to make up a large percentage of cloned sequences recovered from paleolithic paintings. The present study addresses the intraphylum diversity of Acidobacteria in Altamira Cave. In contrast to previous studies, we have focused on 23S rRNA-based phylogenetic analyses, exploiting the high information content of the 23S RNA gene. Comparison with existing studies was facilitated by the preparation of corresponding 16S rRNA clone libraries. Fourty-one distinct operational taxonomic units (OTU) could be identified. Of the eight described acidobacterial subgroups, five were represented in the cave; only subgroups 1, 2, and 8 were not found. Subgroup 4 was the group harbouring the highest number of OTUs. Various clusters that could not be assigned to any of the established subgroups, but were clearly grouped within the phylum and appeared to represent new taxa at elevated phylogenetic levels, were detected. Results from this study give a first insight into the enormous acidobacterial diversity existing in a single hypogean environment containing unique paleolithic paintings, the Altamira Cave. Novel taxa have been found within the phylum, suggesting a higher diversity of Acidobacteria than previously suspected even at a local scale.     

Distribution of Cren- and Euryarchaeota in Scots Pine Mycorrhizospheres and Boreal Forest Humus

Archaeal 16S rRNA gene sequences have been found in a variety of moderate-temperature habitats including soil and rhizospheres. In this study, the differences of archaeal communities associated with Scots pine (Pinus sylvestris L.) short roots, different types of mycorrhizospheric compartments, and uncolonized boreal forest humus were tested by direct DNA extraction, polymerase chain reaction–denaturing gradient gel electrophoresis (PCR–DGGE), and sequencing. The results indicated that mycorrhizal colonization of Scots pine roots substantially influence the archaeal community of pine rhizospheres. Colonization of short roots by most mycorrhizal fungi tested increased both archaeal frequency and diversity. Most of the archaeal sequences encountered in mycorrhizas belonged to the phylum Euryarchaeota, order of Halobacteriales. The difference in archaeal diversity between the mycorrhizospheric compartments and humus was profound. Most compartments with fungal components contained euryarchaeotal 16S rRNA gene sequences, whereas a high diversity of crenarchaeotal sequences and no euryarchaeotal sequences were found in forest humus outside mycorrhizospheres.     

High local and global diversity of Flavobacteria in marine plankton

Members of the phylum Bacteroidetes are among the most abundant microbes in coastal marine waters, but it is unclear to which extent the diversity within this phylum is covered by currently available 16S rRNA gene sequence information. We, thus, obtained a comprehensive collection of sequence types affiliated with Bacteroidetes in coastal North Sea surface waters and we compared this local diversity with the available sequences of marine planktonic and other aquatic Bacteroidetes. Approximately 15% of > 600 clones from two libraries (August 2000, June 2001) were related to Bacteroidetes, specifically to the Flavobacteria. Local diversity appeared to be almost exhaustively sampled. However, the diversity of the two libraries virtually did not overlap, indicating a pronounced temporal variability of the planktonic Flavobacteria assemblage. The majority of sequence types represented novel phylogenetic lineages, adding 6-7% to the currently known genera and species of Bacteroidetes in marine waters. Different diversity estimators suggested that so far only approximately half of the global diversity of planktonic marine Bacteroidetes has been described. The data set moreover indicated that cultivation-independent techniques and isolation approaches have recovered almost equally sized and virtually non-overlapping fractions of the currently known diversity within this phylum. Interestingly, only 15% of genera of Bacteroidetes from various aquatic environments appear to occur in more than one habitat type.     

Molecular analysis of fungal diversity associated with three bryophyte species in the Fildes Region, King George Island, maritime Antarctica

The fungal communities associated with three bryophytes species (the liverwort Barbilophozia hatcheri, the mosses Chorisodontium aciphyllum and Sanionia uncinata) in the Fildes Region, King George Island, maritime Antarctica, were studied using clone library analysis. Fungal communities showed low diversity; the 680 clones belonged to 93 OTUs. Of these, 78 belonged to the phylum Ascomycota, 13 to the phylum Basidiomycota, 1 to the phylum Zygomycota, and 1 to an unknown phylum. Among the OTUs, the most common orders in the Ascomycota were Helotiales (42 OTUs) and Chaetothyriales (14 OTUs) and the most common orders in the Basidiomycota were Sebacinales (3 OTUs) and Platygloeales (3 OTUs). Most OTUs clustered within clades that contained phylotypes identified from samples in Antarctic or Arctic ecosystems or from bryophytes in other ecosystems. In addition, we found that host-related factor may shape the fungal communities associated with bryophytes in this region. This is the first systematic study of the fungal community in Antarctic bryophytes to be performed using culture-independent method and the results may improve understanding of the endophytic fungal evolution and ecology in the Antarctic ecosystem.     

Functional gene diversity analysis in BTEX contaminated soils by means of PCR-SSCP DNA fingerprinting: comparative diversity assessment against bacterial isolates and PCR-DNA clone libraries

Developments in molecular biology based techniques have led to rapid and reliable tools to characterize microbial community structures and to monitor their dynamics under in situ conditions. However, there has been a distinct lack of emphasis on monitoring the functional diversity in the environment. Genes encoding catechol 2,3-dioxygenases (C23O), as key enzymes of various aerobic aromatic degradation pathways, were used as functional targets to assess the catabolic gene diversity in differentially BTEX contaminated environments by polymerase chain reaction-single-strand conformation polymorphism (PCR-SSCP). Site specific PCR-SSCP fingerprints were obtained, showing that gene diversity experienced shifts correlated to temporal changes and levels of contamination. PCR-SSCP enabled the recovery of predominant gene polymorphs, and results closely matched with the information retrieved from random sequencing of PCR-DNA clone libraries. A new method for isolating strains capable of growing on BTEX compounds was developed to diminish preselection or enrichment bias and to assess the function of predominant gene polymorphs. C23O abundance in isolates correlated with the levels of BTEX pollution in the soil samples analysed. Isolates harbouring C23O genes, identical to the gene polymorph predominant in all contaminated sites analysed, showed an unexpected benzene but not toluene mineralizing phenotype whereas isolates harbouring a C23O gene variant differing by a single point mutation and observed in highly polluted sites only, were capable, among some other isolates, to mineralize benzene and toluene, indicating a catabolically determined sharing of carbon sources on-site. The PCR-SSCP technique is thus a powerful tool for assessing the diversity of functional genes and the identification of predominant gene polymorphs in environmental samples as a prerequisite to understand the functioning of microbial communities.     

The Evolution of Tyrosine-Recombinase Elements in Nematoda

Transposable elements can be categorised into DNA and RNA elements based on their mechanism of transposition. Tyrosine recombinase elements (YREs) are relatively rare and poorly understood, despite sharing characteristics with both DNA and RNA elements. Previously, the Nematoda have been reported to have a substantially different diversity of YREs compared to other animal phyla: the Dirs1-like YRE retrotransposon was encountered in most animal phyla but not in Nematoda, and a unique Pat1-like YRE retrotransposon has only been recorded from Nematoda. We explored the diversity of YREs in Nematoda by sampling broadly across the phylum and including 34 genomes representing the three classes within Nematoda. We developed a method to isolate and classify YREs based on both feature organization and phylogenetic relationships in an open and reproducible workflow. We also ensured that our phylogenetic approach to YRE classification identified truncated and degenerate elements, informatively increasing the number of elements sampled. We identified Dirs1-like elements (thought to be absent from Nematoda) in the nematode classes Enoplia and Dorylaimia indicating that nematode model species do not adequately represent the diversity of transposable elements in the phylum. Nematode Pat1-like elements were found to be a derived form of another Pat1-like element that is present more widely in animals. Several sequence features used widely for the classification of YREs were found to be homoplasious, highlighting the need for a phylogenetically-based classification scheme. Nematode model species do not represent the diversity of transposable elements in the phylum.     

Changes in Bacterial Community Structure of Agricultural Land Due to Long-Term Organic and Chemical Amendments

Community level physiological profiling and pyrosequencing-based analysis of the V1-V2 16S rRNA gene region were used to characterize and compare microbial community structure, diversity, and bacterial phylogeny from soils of chemically cultivated land (CCL), organically cultivated land (OCL), and fallow grass land (FGL) for 16 years and were under three different land use types. The entire dataset comprised of 16,608 good-quality sequences (CCL, 6,379; OCL, 4,835; FGL, 5,394); among them 12,606 sequences could be classified in 15 known phylum. The most abundant phylum were Proteobacteria (29.8%), Acidobacteria (22.6%), Actinobacteria (11.1%), and Bacteroidetes (4.7%), while 24.3% of the sequences were from bacterial domain but could not be further classified to any known phylum. Proteobacteria, Bacteroidetes, and Gemmatimonadetes were found to be significantly abundant in OCL soil. On the contrary, Actinobacteria and Acidobacteria were significantly abundant in CCL and FGL, respectively. Our findings supported the view that organic compost amendment (OCL) activates diverse group of microorganisms as compared with conventionally used synthetic chemical fertilizers. Functional diversity and evenness based on carbon source utilization pattern was significantly higher in OCL as compared to CCL and FGL, suggesting an improvement in soil quality. This abundance of microbes possibly leads to the enhanced level of soil organic carbon, soil organic nitrogen, and microbial biomass in OCL and FGL soils as collated with CCL. This work increases our current understanding on the effect of long-term organic and chemical amendment applications on abundance, diversity, and composition of bacterial community inhabiting the soil for the prospects of agricultural yield and quantity of soil.