bornberglab.org

Cheers and congratulations to Bharat! His new paper is about the theory behind the emergence of de novo genes.
New protein coding genes can emerge from genomic regions that previously did not contain any genes, via a process called de novo gene emergence. To synthesize a protein, DNA must be transcribed as well as translated. Both processes need certain DNA sequence features. Stable transcription requires promoters and a polyadenylation signal, while translation requires at least an open reading frame (ORF). We develop mathematical models based on mutation probabilities, and the assumption of neutral evolution, to find out how quickly genes emerge and are lost. We also investigate the effect of the order by which DNA features evolve, and if sequence composition is biased by mutation rate. We rationalize how genes are lost much more rapidly than they emerge, and how they preferentially arise in regions that are already transcribed. Our study not only answers some fundamental questions on the topic of de novo emergence but also provides a modeling framework for future studies.

Together with the KHlab in Prague we published our study on de novo proteins compared to random proteins. De novo gene emergence provides a route for new proteins to be formed from previously non-coding DNA. Proteins born in this way are considered random sequences and typically assumed to lack defined structure. Taking putative de novo proteins identified in human and fly, we experimentally characterize a library of these sequences to assess their solubility and structure propensity. We compare this library to a set of synthetic random proteins with no evolutionary history. Bioinformatic prediction suggests that de novo proteins may have remarkably similar distributions of biophysical properties to unevolved random sequences of a given length and amino acid composition. However, upon expression in vitro, de novo proteins exhibit moderately higher solubility which is further induced by the DnaK chaperone system. We suggest that while synthetic random sequences are a useful proxy for de novo proteins in terms of structure propensity, de novo proteins may be better integrated in the cellular system than random expectation, given their higher solubility.

Happy to announce that the lab just received its 4th HFSP grant! “New Kids on the Block: how De Novo emerged micropeptides rewire cellular networks”. This time with Anne-Ruxandra Carvunis and Christine Brun. HFSP Awards 2023

Last week our group participated in the second Münster Evolution Meeting (MEM). There were many interesting talks and great posters and we were lucky to meet so many great people. It was a nice conference and many of us had the opportunity to present their research in a talk (like Anna Grandchamp here in the picture) or during the poster sessions. We want to thank the organising team from the Gadau group again and hope to see everyone again at the next MEM!

For one exciting month we have a guest researcher from Zagreb, Croatia in our group. Aleksandra Marsavelski is visiting us as a WiRe fellow to look at plastic degrading enzymes. Together with our group she wants to reconstruct ancestors of enzymes with a known plastic degrading activity and enhance their function. This can help us in the future to recycle plastics in an environmentally friendly way. For more information and news, check out the WiRe website of the University here.

In this commentary we discuss the recent paper from Alvarez-Carreño et al. about the evolution of new folds. In particular, we look at ancient folds from the dawn of the RNA-protein world and how new and still existing folds may have originated through reshaping of the old folds. The mechanism introduced by Alvarez-Carreño et al., called "creative Destruction" describes the process of innovation through the “destruction” of an old product and thereby generating a new one. An analogy from everyday life is the development of an mp3 player from a cassette player. The old cassette player, lost its overall form and the need of a cassette tape to develop into an mp3 player. Form and function of both products are similar while some aspects of the ancestral product have been ‘destroyed’, i.e. cassette, bulky structure and loudspeaker, to create the new features, i.e. memory space, small, headphones.

Mark and Bertrand are organising the first international Blattodea Conference in Münster. The Conference will take place in the Castle from 3rd to 4th of April. Registrations are open under Indico. We look forward to seeing you in Münster soon.

Our Master student Kai has succesfully defended his Thesis last December on "Structural analysis of putative de novo protein Atlas and its ancestors". After mastering many obstacles in the wet lab, Kai found his true calling during the computational analyses. Now he is heading off to new computational adventures and we wish him all the best of luck on his journey!

Birte Höcker from the University of Bayreuth gave an IEB seminar on the Evolution and Design of Protein Folds. Thanks for visiting our group and the IEB!

We had a great symposium at the Xplanatorium in Hanover Herrenhausen from the 29th to 30th of November. Together with our collaborators Ylva Ivarsson from Uppsala, Florian Hollfelder from Cambridge and Klara Hlouchova from Prague we look into the early evolution of proteins from random sequence space. Our project on the emergence of new proteins by de novo mechanism is funded by the Volkswagen Stiftung Life? initiative together with several other interesting projects.

We are happy to announce that MEM is finally back! See you all in Münster from 13th -16th March 2023. The Münster Evolution Meeting (MEM) aims to provide a forum for all Evolutionary Biologists working across different fields. Besides having the opportunity to share and learn about excellent research in evolutionary biology MEM also aims at bringing together Evolutionary Biologists working in German-speaking countries in a smaller setting, to allow for intensive networking and discussion. Münster is a welcoming and vibrant university town, offering a perfect venue. It was the home of Prof. Dr. Bernhard Rensch, who contributed significantly to the “Modern Evolutionary Synthesis”. Click here to register!

Using available genome and transcriptome of cockroaches and termites as well as de novo transposon annotations, our study brings further evidence on the role of transposon-aided adaptations during termite eusocial transition. Our study reveals that transposon insertions within differentially expressed genes (DEGs) among castes in termites and life-stages (corresponding to termite castes) in cockroaches display opposite patterns. Furthermore, while in cockroaches transposon families do not differ in their insertion frequency within DEGs, retrotransposon and DNA transposon insertions are more frequent in worker- and queen-biased genes, respectively. In addition, the insertion of transposons in queen-biased genes in termites are more frequent in genes involved in reproduction, ageing, and immunity, functions essential for queen phenotype; while transposon insertion in termite worker-biased genes are more frequent in genes involved in the regulation of gene expression and behaviour, functions associated with phenotypic plasticity and the apparition of a sterile caste. In conclusion, our study highlights the role of transposon during the eusocial transition in Blattodea, potentially through shifts in gene expression.

After Sarah's successful Master thesis defence we had some delicious Flammkuchen together with her family. The title of her thesis was "The role of selection in the emergence of caste-biased genes in termites" and she was under the amazing supervision of Mark. We are very happy that she now started her PhD in the group on the evolutionary genomics of sociality in beetles funded by GEvol (SPP 2349)

Here we examined proteomes of 21 chordates, of which 18 are vertebrates, to reveal the modular evolution of the blood coagulation cascade. Within the vertebrate coagulation protein set, almost half of the studied proteins are shared with jawless vertebrates. Domain similarity analyses revealed that there are multiple possible evolutionary trajectories for each coagulation protein. During the evolution of higher vertebrate clades, gene and genome duplications led to the formation of other coagulation cascade proteins.

We just got back from our awesome second group retreat this year! A lot of great presentations and talks, especially from and with our special guest Richard Goldstein. Apart from the serious scientific topics, we went for a beautiful walk to see the famous "Küssende Sau" (kissing pig). Stay tuned for more pictures...

The kick-off meeting for the DFG Priority Programme “Genomic Basis of Evolutionary Innovations (GEvol)” (SPP 2349) coordinated by Erich was the first in-person meeting of nearly all of the 40 involved PIs! The goal of the Priority Programme is to exploit new methods to reveal in the insect taxon the role of: coding vs. regulatory changes, transposable elements, epigenetic regulation, gene family evolution, copy number dynamics, structural genomic rearrangements etc. in trait evolution by using multiple cutting edge quantitative OMICs resources (e.g. genomics, transcriptomics and epigenomics). Eventually, the emerging hypotheses shall be tested by functional genetics experiments where possible.

In this article we compare different methods to sort large libraries of enzymes presented on the surface of E. coli, and recovering the intact cells without lysis. We changed a protocol in which single cells encapsulated in a microdroplet are measured using Fluorescence-activated droplet sorting (FADS) to a protocol were cells are grown inside a microdroplet after encapsulation of a single cell, resulting in multiple copies of the same variant inside each droplet. We find that growing cells inside a microdroplet prior to FADS increases both the amount of cells recovered as well as reducing the amount of false positives.

This time the group leader Erich Bornberg-Bauer himself presented our work on the role of transposable elements in termites. The 21st HFSP Awardees meeting took place in beautiful Paris this year. The poster is based on work by postdoc Mark Harrison and former postdoc Evelien Jongepier from our group in cooperation with Mireille Vasseur-Cognet (Paris), Hei Sook Sul (Berkeley) and Wilhelm de Beer (Pretoria).
We compared whole-genome levels of repeat element transcription in the fat body of female workers, kings, and five different queen stages. Those queens can live over 20 years, maintaining near maximum reproductive output! The sterile workers only live weeks or months. We found substantially higher TE activity in workers than in reproductives. Furthermore, relative TE expression decreased with age in queens, due to a significant upregulation of the PIWI-pathway in 20-year-old queens. Our results suggest a caste- and age-specific regulation of the PIWI-pathway has evolved in higher termites that is analogous to germ-line-specific activity in individual organisms, promoting reproductive fitness even at high age.

The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste exhibits highly specialized morphology, behaviour, and life-history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making ants. Here, we investigate whether gene expression varies in parallel ways between lifestyles (slave-making versus host ants) across five independent origins of ant slavery in the “Formicoxenus-group” of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave-making ants than in nonparasitic ants, we also compare caste-specific gene expression patterns between lifestyles. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste-associated modules of coexpressed genes with strong connectivity. However, several genes and one gene module are linked to slave-making across the independent origins of this parasitic lifestyle, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences in gene expression remain consistent even when species switch to a parasitic lifestyle. Our findings strongly support the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, as proposed by the “genetic toolkit” hypothesis.

Our postdoc Anna Grandchamp presented her poster on proto-gene emergence and PhD student Alina Mikhailova gave a talk about domain rearrangements in social termites. Awesome work by both of them!

Our postdoc Mark C Harrison presented his work on social insects this week on the International Congress of Entomology (ICE) in Helsinki, Finnland. Check out his latest publications in Open Biology and Genome Biology and Evolution

The reproductive castes of eusocial insects are often characterized by extreme lifespans and reproductive output, indicating an absence of the fecundity/ longevity trade-off. The role of DNA methylation in the regulation of caste- and age-specific gene expression in eusocial insects is controversial. While some studies find a clear link to caste formation in honeybees and ants, others find no correlation when replication is increased across independent colonies. Although recent studies have identified transcription patterns involved in the maintenance of high reproduction throughout the long lives of queens, the role of DNA methylation in the regulation of these genes is unknown. We carried out a comparative analysis of DNA methylation in the regulation of caste-specific transcription and its importance for the regulation of fertility and longevity in queens of the higher termite Macrotermes natalensis. We found evidence for significant, well-regulated changes in DNA methyl- ation in mature compared to young queens, especially in several genes related to ageing and fecundity in mature queens. We also found a strong link between methylation and caste-specific alternative splicing. This study reveals a complex regulatory role of fat body DNA methylation both in the div- ision of labour in termites, and during the reproductive maturation of queens.

Today, we know that proteins do not only evolve by duplication and divergence of existing proteins but also arise from previously non-coding DNA. These proteins are called de novo proteins. Their properties are still poorly understood and their experimental analysis faces major obstacles. Here, we aim to present a starting point for soluble expression of de novo proteins with the help of chaperones and thereby enable further characterization.
Over the past decade, evidence has accumulated that new protein-coding genes can emerge de novo from previously non-coding DNA. Most studies have focused on large scale computational predictions of de novo protein-coding genes across a wide range of organisms. In contrast, experimental data concerning the folding and function of de novo proteins are scarce. This might be due to difficulties in handling de novo proteins in vitro, as most are short and predicted to be disordered. Here, we propose a guideline for the effective expression of eukaryotic de novo proteins in Escherichia coli. We used 11 sequences from Drosophila melanogaster and 10 from Homo sapiens for heterologous expression. The candidate de novo proteins have varying secondary structure and disorder content. Using multiple combinations of purification tags, E. coli expression strains, and chaperone systems, we were able to increase the number of solubly expressed putative de novo proteins from 30% to 62%. We found that, overall, proteins with higher predicted disorder were easier to express.

Our PhD student Lars and Janina Rinke from the lab of Jürgen Gadau were elected as IEB student representatives for the next two years!

Our dear student Christopher Finke has successfully defended his Master thesis yesterday evening. Supervised by Alice Séguret he looked into differences between slave-maker ants and their host species and was able to generate valuable genome annotations. Christopher started out as a Bachelor student in the lab with us and moved on to computational work during his Master studies. Congratulations and good luck in Berlin!

The use of environmental DNA as a proxy to identify species has increased exponentially in the last few years. However, how good eDNA relates with actual species presence/abundance remains elusive. Our study fill this gap, comparing both soil eDNA and visual assessments of plants in Norway. It shows that soil eDNA allows to describe well local plant biodiversity, with an average 60% match with visual survey for vascular plants, and also to recover past vegetation biodiversity. Our soil eDNA method then provide a great tool to assess rapidly plant biodiversity in any seasons.

Our PhD students Margaux Aubel and Lars Eicholt presented their most recent work on soluble expression of putative de novo proteins at Apfed22 in Bayreuth! If you did not attend, please check out their preprints here and here. We would like to thank all the organizers for this amazing hybrid conference. The speaker line-up was diverse both in backgrounds and research areas, while reaching gender parity!

Some insects are eusocial, which means that their society is organized into different castes which carry out specific colony tasks. In termites, for example, the “king” and the “queen” are involved in reproduction, while the “workers” are involved in resource gathering and brood-care. Macrotermes natalensis is a species of higher termite that creates large complex colonies, in which the king and the queen (reproductives) have a long life, spanning decades, and the queen remains highly fertile throughout her adult life. Workers, on the other hand, are short-lived and sterile. We studied this species of termites, using a combination of high throughput techniques such as transcriptomics, metabolomics and lipidomics, to identify mechanisms that allow reproductives to live orders of magnitude longer than workers, while maintaining high fertility. Aging associated genes were differentially expressed between the reproductives and the workers. For example, antioxidant genes were highly expressed, and the membrane lipids were less damaged by oxidative stress, in the queens relative to workers. Contrary to expectations, we found that several members of the insulin/insulin-like growth factor signaling (IIS) pathway were upregulated in the queens. Normally this would indicate increased diversion of metabolism towards energy storage. However, we did not find excessive fat storage in the queens; simple sugars dominate in their hemolymph and a large amount of resources is allocated to egg production. Our findings support the notion that aging results from a complex interplay of several processes. These processes should be studied simultaneously and not in isolation, for a better understanding of aging.