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• W4308293775 abstract "One of the most conspicuous examples of evolution in action is the awesome spectacle of how environmental microorganisms manage to face and eventually metabolize xenobiotic compounds with synthetic chemical structures that have not been in the Biosphere before we release them—in many cases with bad long-term consequences. Along with the onset of antibiotic resistances, emergence of new metabolic capabilities is one of the exemplary cases of real-time appearance of new activities in the biological world. Just to raise an example: when artificial sweetener acesulfame (ACE) was first introduced it was considered to be altogether recalcitrant to any biological action. Yet, years later, bacterial biodegradation was reported and a just a bit later, ACE-degrading strains were found all over the world bearing a defined pathway for its metabolization (Castronovo et al., 2017). In reality, the factual concentrations of ACE in waste-water treatment plants are very low and thus the selective pressure to leverage the as a nutrient is generally mild. Under such circumstances, what drove the emergence of a new pathway? What were the intermediate steps from no-degradation to full degradation? The traditional view on the rise of novel traits in biological systems affirms that newness is determined by both access to genetic variation and exposure to different ecological opportunities. The genetics behind range expansions is shaped by the interplay between Darwinian selection and random genetic drift at the margins. The dynamics of the process is highly sensitive to fluctuations induced by environmental heterogeneities (Gralka & Hallatschek, 2019). This suffices to account for most of the multi-scale diversity and emergence of new activities of the extant biological world but also it leaves aside three important questions which become also factual limitations. First, for a gene to acquire a new function there should be already a precursor sequence from which it can evolve. In other words, every new activity often starts with duplication and separate diversification of an already existing DNA segment in a fashion that enables the shaping of the new trait at no fitness cost (Lundin et al., 2020). Yet, it has been calculated that the number of naturally occurring 100 amino acid residues sequences (Huang et al., 2016) is in the range of 1015. This is a large number, but altogether insignificant as compared to the number of possible sequences (20100 = 1.3 × 10130). That emergence of new functions depends on genetic drifts at the margins of an existing gene leaves empty an enormous DNA sequence space for creation of truly novel functions. The detectable diversity of the biological world is thus the result of historical contingencies, leaving vast sequence landscapes with an immense functional potential entirely virgin (Terra Incognita, Figure 1). A second feature is the standard view that the main—if not the only—driver of Darwinian evolution is reproductive advantage. In the case of emergence of complex traits, the prevailing explanation is that every temporary stage prior to the surfacing of a new function is endowed also of an inconspicuous but still effective fitness benefit (Dawkins, 1997). That is, intermediate steps before the phenotype of interest emerges do deliver some—if subtle—advantage which enables subsequent steps of the evolutionary process. But in the cases where there is a long evolutionary roadmap until gaining a new propagative ability, such interim evolutionary stages are often hard to identify. The question thus arises on whether—for the sake of exploring a wider range of itineraries—other drivers of evolution can be implemented prior to new traits resulting in improved proliferation of the host. Finally, the merge of Darwinian theory with the Central Dogma of Molecular Biology implies that the one and only source of biological novelty is changes in DNA, which then propagate uni-directionally all the way to a manifest phenotype. However, it has become growingly clear that errors in transcription and translation in single cells originate a much wider phenotypic diversity in a population than that borne by its genetic complement (Evans et al., 2018; Gamba & Zenkin, 2018; Li & Lynch, 2020; Ninio, 1991, 1997). Some of these errors can create transient properties that enable survival of individual hosts. It would not be economical that once a molecular solution to a challenge has been found, it is lost because it does not stem from DNA mutations. Can such momentary advantages be eventually imprinted in the genome? By the same token, a large number of recognizable metabolic reactions, for example, pentoses cycle (Luisi, 2014) happen to occur abiotically much before they were encoded genetically. Were such—now biotic—cycles re-invented or somehow adopted by evolving biological systems? In sum, standard evolutionary theory basically accounts for the phenomenon of innovation (doing something different on the basis of co-opting and repurposing the existing). But in this Crystal Ball, I would argue that it generally fails to account for novelty, which is about emergence of something entirely new (Wagner, 2011). Lucretious' famous aforism ex nihilo nihil fit (nothing comes from nothing) needs to be qualified when discussing emergence of biological activities. These issues are not just merely academic or speculative questions as they determine our understanding and management of very practical matters, from evolution of antibiotic resistances to setting adaptive laboratory evolution experiments (Sandberg et al., 2019) for biotechnological purposes. Mostly due to the frequent appearance of antibiotic resistances, it is generally believed that bacteria quickly evolve new genes and functions (Knopp et al., 2019). But this is only a half-truth. Prokaryotes are extraordinarily innovative to repurpose existing genes and DNA sequences upon genetic drift (see above). But their genomes are typically packed with functional genes, so virtually all sequences are busy with already assigned roles. This makes extant bacteria poor creators of novelty, as their exploration of the solution space to given problems is limited to making variants of already existing bits and parts of their genomic complement. In contrast, it might not be casual that higher eukaryotes capitalize on their (so-called) junk DNA to evolve genuinely novel genes (Baalsrud et al., 2017; Biémont & Vieira, 2006a). Such non-assigned DNA can enable exploration of sequences that are far from the ones already delivering given functions and therefore do not require duplications of otherwise assigned sequences/functions for exploring new functional landscapes. The archetypal roadmap of how a genuinely newborn gene comes to existence begins with a non-coding DNA sequence that undergoes changes, which enable it to be transcribed, translated and potentially confer a new function (Blevins et al., 2021). While it may appear counterintuitive that random variations in a non-coding DNA may end up in a bona fide gene delivering a beneficial trait, evidence does exist that this is the case in a considerable number of instances. However, it is in fact perplexing that de novo gene birth (i.e., creation of new genes from otherwise non-coding DNA sequences) has hardly been investigated in bacteria: Virtually all studies on the issue have taken place in eukaryotic cells and animals (Ruiz-Orera et al., 2020). The ensuing question is whether extant bacteria, often assumed to be the most creative biological actors, are in fact the ones able to generate authentic novelty at the current stage of the evolutionary history. This is because apart of pseudogenes and ex-genes (generally tagged as junk DNA; Biémont & Vieira, 2006a), existing prokaryotic genomes conspicuosly lack what one could call pristine sequences that could be subject to a process of genification. Also, note that prokaryotes have a clear deletional bias that eliminates junk DNA, so there is less grounds for keeping non-assigned sequences usable later as an evolutionary resource. This does not mean that prokaryotes cannot generate novelty. While some bacteria carry what look like stable genomes, other carry islands with much (apparently) non-functional DNA. Furthermore, they often bear long segments of intergenic DNA that can be the source of new roles. Also, existing genes can be overprinted to generate fresh functions (Delaye et al., 2008). Finally, bacteria do benefit from the immense traffic of DNA sequences mediated by phages and other types of horizontal gene transfer as part of their innovation repertoire. But how does this compare to eukaryotes, which often have so much more non-coding DNA to start with, that is, more fresh genetic material for evolution (Levy, 2019)? True, it is difficult to ascertain how much eukaryotic non-coding DNA was never coding, as genes and sequences first defined as orphan were found not to be when more genomes were sequenced, for example, stemming from dead transposable elements, etc. But in any case, it looks like eukaryotes have a better headstart for novelty as they have a better reservoir of once-functional sequences. Such sequences can indeed originate new genes, for example, domain fusion (Warsi et al., 2020). Eukaryotes can also benefit from viral traffic of DNA, including inter-kingdom exchanges. But in my opinion, the key to understand genuine biological novelty is understanding how a random DNA segment becomes a functional gene. In other words, how a sequence devoid of any upfront meaning captures information (Ohno & Epplen, 1983). Perhaps this is not unlike a random association of sounds end up being an information-bearing word: May there be lessons to learn from computational linguistics (Miller et al., 2022)? What specifically all these (very incomplete) disgressions on the birth of new genes mean for the sake of this Crystal Ball? My point is that we often leave behind and move ahead believing that we know enough of a given fundamental issue for carrying on. I have been through dozens, if not hundreds of papers using experimental laboratory evolution (ALE) applied to a single bacterial strain, pathway or gene for generating new biological activities: We run ALE it in our own Laboratory at all times (Espeso et al., 2021). The good part is that ALE indeed results in fresh properties that cannot be engineered rationally. The downside is that—because of the reasons above—ALE generally delivers innovation, not novelty. By focusing in single bacterial strains as the subject of experimental evolution we miss a good part of the possible solution space to a given evolutionary challenge. There is thus plenty of room for exploring both theoretically and practically the power of evolution to surf a way denser solution space than the one currently entertained. Existing bacteria may not be the best starting point for the pursuit of novelty. We may need to develop specific biological platforms, for example, evolving prokaryotic/eukaryotic consortia that capture and recreate more mechanisms of gene birth than the ones available in single bacteria. By replaying evolutionary itineraries and generating entirely new catalytic activities such evolving consortia might in fact be the key for addressing some of the phenomenal challenges that afflict us as the result of climate change and massive environmental deterioration. Much of the contents of this Crystal Ball were inspired by a Twitter discussion on the birth of new genes that took place in September–October 2022 elicited by https://twitter.com/vdlorenzo_CNB/status/1575462066734907397. Víctor de Lorenzo is grateful to all those who participated in the conversation. The work in Author's Laboratory is funded by the SYCOLIM (ERA-COBIOTECH 2018–PCI2019-111859-2 of MCIN/AEI/10.13039/501100011033/EU) Projects of the Spanish Ministry of Science and Innovation, SYNBIO4FLAV (H2020-NMBP-TR-IND/H2020-NMBP-BIO-2018-814650) and MIX-UP (MIX-UP H2020-BIO-CN-2019-870294) Contracts of the European Union and the BIOSINT-CM (Y2020/TCS- 6555) Projects of the Comunidad de Madrid—European Structural and Investment Funds (FSE, FECER). The author declares no conflict of interest." @default.
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• W4308293775 title "Innovation versus novelty in microbial systems" @default.
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