Phylogenetic divergence between the obligate luminous symbionts of flashlight fishes demonstrates specificity of bacteria to host genera

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/107544/1/emi412135.pd

Genome Evolution in the Obligate but Environmentally Active Luminous Symbionts of Flashlight Fish

The luminous bacterial symbionts of anomalopid flashlight fish are thought to be obligately dependent on their hosts for growth and share several aspects of genome evolution with unrelated obligate symbionts, including genome reduction. However, in contrast to most obligate bacteria, anomalopid symbionts have an active environmental phase that may be important for symbiont transmission. Here we investigated patterns of evolution between anomalopid symbionts compared with patterns in free-living relatives and unrelated obligate symbionts to determine if trends common to obligate symbionts are also found in anomalopid symbionts. Two symbionts, ?Candidatus Photodesmus katoptron? and ?Candidatus Photodesmus blepharus,? have genomes that are highly similar in gene content and order, suggesting genome stasis similar to ancient obligate symbionts present in insect lineages. This genome stasis exists in spite of the symbiont?s inferred ability to recombine, which is frequently lacking in obligate symbionts with stable genomes. Additionally, we used genome comparisons and tests of selection to infer which genes may be particularly important for the symbiont?s ecology compared with relatives. In keeping with obligate dependence, substitution patterns suggest that most symbiont genes are experiencing relaxed purifying selection compared with relatives. However, genes involved in motility and carbon storage, which are likely to be used outside the host, appear to be under increased purifying selection. Two chemoreceptor chemotaxis genes are retained by both species and show high conservation with amino acid sensing genes, suggesting that the bacteria may actively seek out hosts using chemotaxis toward amino acids, which the symbionts are not able to synthesize

Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes

Diverse marine fish and squid form symbiotic associations with extracellular bioluminescent bacteria. These symbionts are typically free-living bacteria with large genomes, but one known lineage of symbionts has undergone genomic reduction and evolution of host dependence. It is not known why distinct evolutionary trajectories have occurred among different luminous symbionts, and not all known lineages previously had genome sequences available. In order to better understand patterns of evolution across diverse bioluminescent symbionts, we de novo sequenced the genomes of bacteria from a poorly studied interaction, the extracellular symbionts from the “lures” of deep-sea ceratioid anglerfishes. Deep-sea anglerfish symbiont genomes are reduced in size by about 50% compared to free-living relatives. They show a striking convergence of genome reduction and loss of metabolic capabilities with a distinct lineage of obligately host-dependent luminous symbionts. These losses include reductions in amino acid synthesis pathways and abilities to utilize diverse sugars. However, the symbiont genomes have retained a number of categories of genes predicted to be useful only outside the host, such as those involved in chemotaxis and motility, suggesting that they may persist in the environment. These genomes contain very high numbers of pseudogenes and show massive expansions of transposable elements, with transposases accounting for 28 and 31% of coding sequences in the symbiont genomes. Transposon expansions appear to have occurred at different times in each symbiont lineage, indicating either independent evolutions of reduction or symbiont replacement. These results suggest ongoing genomic reduction in extracellular luminous symbionts that is facilitated by transposon proliferations

Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment

Deep-sea anglerfishes are relatively abundant and diverse, but their luminescent bacterial symbionts remain enigmatic. The genomes of two symbiont species have qualities common to vertically transmitted, host-dependent bacteria. However, a number of traits suggest that these symbionts may be environmentally acquired. To determine how anglerfish symbionts are transmitted, we analyzed bacteria-host codivergence across six diverse anglerfish genera. Most of the anglerfish species surveyed shared a common species of symbiont. Only one other symbiont species was found, which had a specific relationship with one anglerfish species, Cryptopsaras couesii. Host and symbiont phylogenies lacked congruence, and there was no statistical support for codivergence broadly. We also recovered symbiont-specific gene sequences from water collected near hosts, suggesting environmental persistence of symbionts. Based on these results we conclude that diverse anglerfishes share symbionts that are acquired from the environment, and that these bacteria have undergone extreme genome reduction although they are not vertically transmitted

Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps

Ecological constraints on independent breeding are recognised as major drivers of cooperative breeding across diverse lineages. How the prevalence and degree of cooperative breeding relates to ecological variation remains unresolved. Using a large data set of cooperative nesting in Polistes wasps we demonstrate that different aspects of cooperative breeding are likely to be driven by different aspects of climate. Whether or not a species forms cooperative groups is associated with greater short‐term temperature fluctuations. In contrast, the number of cooperative foundresses increases in more benign environments with warmer, wetter conditions. The same data set reveals that intraspecific responses to climate variation do not mirror genus‐wide trends and instead are highly heterogeneous among species. Collectively these data suggest that the ecological drivers that lead to the origin or loss of cooperation are different from those that influence the extent of its expression within populations.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/113673/1/ele12488.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/113673/2/ele12488_am.pd

Characterization of the microbiome and bioluminescent symbionts across life stages of ceratioid anglerfishes of the gulf of mexico

The interdependence of diverse organisms through symbiosis reaches even the deepest parts of the oceans. As part of the DEEPEND project (deependconsortium.org) research on deep Gulf of Mexico biodiversity, we profiled the bacterial communities (‘microbiomes’) and luminous symbionts of 36 specimens of adult and larval deep-sea anglerfishes of the suborder Ceratioidei using 16S rDNA. Transmission Electron Microscopy was used to characterize the location of symbionts in adult light organs (esca). Whole larval microbiomes, and adult skin and gut microbiomes, were dominated by bacteria in the genera Moritella and Pseudoalteromonas genera. 16S rDNA sequencing results from adult fishes corroborate the previously published identity of ceratioid bioluminescent symbionts and support findings that these symbionts do not consistently exhibit host specificity at the host family level. Bioluminescent symbiont amplicon sequence variants (ASVs) were absent from larval ceratioid samples, but were found at all depths in the seawater, with a highest abundance found at mesopelagic depths. As adults spend the majority of their lives in the meso and bathypelagic, the trend in symbiont abundance is consistent with their life history. These findings support the hypothesis that bioluminescent symbionts are not present throughout host development, and that ceratioids acquire their bioluminescent symbionts from the environment

Angiosperm phylogeny inferred from sequences of four mitochondrial genes

An angiosperm phylogeny was reconstructed in a maximum likelihood analysis of sequences of four mitochondrial genes, atp1, matR, nad5 , and rps3 , from 380 species that represent 376 genera and 296 families of seed plants. It is largely congruent with the phylogeny of angiosperms reconstructed from chloroplast genes atpB, matK , and rbcL , and nuclear 18S rDNA. The basalmost lineage consists of Amborella and Nymphaeales (including Hydatellaceae). Austrobaileyales follow this clade and are sister to the mesangiosperms, which include Chloranthaceae, Ceratophyllum , magnoliids, monocots, and eudicots. With the exception of Chloranthaceae being sister to Ceratophyllum , relationships among these five lineages are not well supported. In eudicots, Ranunculales, Sabiales, Proteales, Trochodendrales, Buxales, Gunnerales, Saxifragales, Vitales, Berberidopsidales, and Dilleniales form a basal grade of lines that diverged before the diversification of rosids and asterids. Within rosids, the COM (Celastrales–Oxalidales–Malpighiales) clade is sister to malvids (or rosid II), instead of to the nitrogen-fixing clade as found in all previous large-scale molecular analyses of angiosperms. Santalales and Caryophyllales are members of an expanded asterid clade. This study shows that the mitochondrial genes are informative markers for resolving relationships among genera, families, or higher rank taxa across angiosperms. The low substitution rates and low homoplasy levels of the mitochondrial genes relative to the chloroplast genes, as found in this study, make them particularly useful for reconstructing ancient phylogenetic relationships. A mitochondrial gene-based angiosperm phylogeny provides an independent and essential reference for comparison with hypotheses of angiosperm phylogeny based on chloroplast genes, nuclear genes, and non-molecular data to reconstruct the underlying organismal phylogeny.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/79100/1/JSE_97_sm_FigS2-1.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/79100/2/JSE_97_sm_FigS2-2.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/79100/3/JSE_97_sm_FigS3.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/79100/4/j.1759-6831.2010.00097.x.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/79100/5/JSE_97_sm_FigS1.pd

Reconstructing the basal angiosperm phylogeny: evaluating information content of mitochondrial genes

Three mitochondrial (atp1, matR, nad5), four chloroplast (atpB, matK, rbcL, rpoC2), and one nuclear (18S) genes from 162 seed plants, representing all major lineages of gymnosperms and angiosperms, were analyzed together in a supermatrix or in various partitions using likelihood and parsimony methods. The results show that Amborella + Nymphaeales together constitute the first diverging lineage of angiosperms, and that the topology of Amborella alone being sister to all other angiosperms likely represents a local long branch attraction artifact. The monophyly of magnoliids, as well as sister relationships between Magnoliales and Laurales, and between Canellales and Piperales, are all strongly supported. The sister relationship to eudicots of Ceratophyllum is not strongly supported by this study; instead a placement of the genus with Chloranthaceae receives moderate support in the mitochondrial gene analyses. Relationships among magnoliids, monocots, and eudicots remain unresolved. Direct comparisons of analytic results from several data partitions with or without RNA editing sites show that in multigene analyses, RNA editing has no effect on well supported relationships, but minor effect on weakly supported ones. Finally, comparisons of results from separate analyses of mitochondrial and chloroplast genes demonstrate that mitochondrial genes, with overall slower rates of substitution than chloroplast genes, are informative phylogenetic markers, and are particularly suitable for resolving deep relationships.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/147147/1/tax25065680.pd

Genome Reduction and Evolution in an Obligate Luminous Symbiont.

The luminous bacteria symbiotic with anomalopid flashlight fish are unusual compared to other luminous symbionts; they cannot be cultured outside the host and are thought to be obligately dependent on their hosts. The aims of this dissertation are to test if anomalopid symbionts are obligately dependent on hosts for growth and to compare the evolutionary history of anomalopid symbionts to symbionts with varying lifestyles. To do this, I present the sequenced genomes of two species of anomalopid symbionts, which I show to have specific interactions with different host species. I find that anomalopid symbionts are obligately dependent on their hosts and that this interaction has had a large affect on their evolution. While anomalopid symbionts are closely related to facultative luminous symbionts, they have multiple characteristics in common with obligate intracellular symbionts. Anomalopid symbionts have reduced genomes due to gene loss. Gene loss has lead to their inability to synthesize most amino acids and to utilize carbon/energy sources besides glucose. The observation of these metabolic deficiencies supports the obligate dependence of anomalopid symbionts on their hosts. I also find patterns consistent with anomalopid symbionts experiencing high levels of genetic drift. For instance, anomalopid symbionts are evolving at a faster rate than free-living relatives. Additionally, anomalopid symbionts are genetically monomorphic, even across a wide geographic range, and have an excess of rare substitutions. Furthermore, one symbiont species displays a high number of nonsynonymous substitutions. These indications of high genetic drift are consistent with the symbionts undergoing population bottlenecks during transfers between host generations. I also find that the two symbiont species are very similar in gene content but highly divergent at both the nucleotide and amino acid level. This finding is comparable to trends seen in obligate intracellular symbionts. The genomic patterns common to obligate intracellular symbionts are caused by their being intracellular and vertically transmitted, thus it is surprising that the extracellular, environmentally acquired symbionts of flashlight fish would also show so many of these trends. That these commonalities exist between symbionts with different ecologies highlights the importance of host interactions in determining the evolutionary history of symbionts.PHDEcology and Evolutionary BiologyUniversity of Michigan, Horace H. Rackham School of Graduate Studieshttp://deepblue.lib.umich.edu/bitstream/2027.42/94077/1/thendry_1.pd