Reusable building blocks in biological systems

One of the most widely recognized features of biological systems is their modularity. The modules that constitute biological systems are said to be redeployed and combined across several conditions, thus acting as building blocks. In this work, we analyse to what extent are these building blocks reusable as compared with those found in randomized versions of a system. We develop a notion of decompositions of systems into phenotypic building blocks, which allows them to overlap while maximizing the number of times a building block is reused across several conditions. Different biological systems present building blocks whose reusability ranges from single use (e.g. condition specific) to constitutive, although their average reusability is not always higher than random equivalents of the system. These decompositions reveal a distinct distribution of building block sizes in real biological systems. This distribution stems, in part, from the peculiar usage pattern of the elements of biological systems, and constitutes a new angle to study the evolution of modularity.

[1]  M. Newman,et al.  Finding community structure in networks using the eigenvectors of matrices. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[2]  K. Niklas,et al.  Dynamical patterning modules in plant development and evolution. , 2012, The International journal of developmental biology.

[3]  Richard M. Karp,et al.  Discovering local structure in gene expression data: the order-preserving submatrix problem , 2002, RECOMB '02.

[4]  Richard M. Karp,et al.  Discovering local structure in gene expression data: the order-preserving submatrix problem. , 2003 .

[5]  Mike E. Davies,et al.  Parsimonious dictionary learning , 2009, 2009 IEEE International Conference on Acoustics, Speech and Signal Processing.

[6]  Gowtham Atluri,et al.  Putting genetic interactions in context through a global modular decomposition. , 2011, Genome research.

[7]  Víctor Mireles,et al.  Minimum-overlap Clusterings and the Sparsity of Overcomplete Decompositions of Binary Matrices , 2015, ICCS.

[8]  Gerhard Schlosser,et al.  Modularity and the units of evolution , 2002, Theory in Biosciences.

[9]  Alistair Rogers,et al.  Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants , 2008, BMC Systems Biology.

[10]  Wentian Li,et al.  Size distribution of function-based human gene sets and the split–merge model , 2016, Royal Society Open Science.

[11]  Sergei Maslov,et al.  Universal distribution of component frequencies in biological and technological systems , 2013, Proceedings of the National Academy of Sciences.

[12]  D. Koller,et al.  A module map showing conditional activity of expression modules in cancer , 2004, Nature Genetics.

[13]  Shlomo Havlin,et al.  Scaling law in sizes of protein sequence families: From super‐families to orphan genes , 2003, Proteins.

[14]  A. Barabasi,et al.  Hierarchical Organization of Modularity in Metabolic Networks , 2002, Science.

[15]  H. Simon,et al.  Near decomposability and the speed of evolution , 2002 .

[16]  Susumu Goto,et al.  Extraction of phylogenetic network modules from prokayrote metabolic pathways. , 2004, Genome informatics. International Conference on Genome Informatics.

[17]  Sean R. Davis,et al.  NCBI GEO: archive for functional genomics data sets—update , 2012, Nucleic Acids Res..

[18]  J. Hopfield,et al.  From molecular to modular cell biology , 1999, Nature.

[19]  S. Bergmann,et al.  The evolution of gene expression levels in mammalian organs , 2011, Nature.

[20]  S. Gould,et al.  Exaptation—a Missing Term in the Science of Form , 1982, Paleobiology.

[21]  H. Crichton-Miller.  Adaptation , 1926 .

[22]  Michael W. Berry,et al.  Algorithms and applications for approximate nonnegative matrix factorization , 2007, Comput. Stat. Data Anal..

[23]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.

[24]  Stuart A Newman,et al.  Dynamical patterning modules: a "pattern language" for development and evolution of multicellular form. , 2009, The International journal of developmental biology.

[25]  S. Bustin.  Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. , 2000, Journal of molecular endocrinology.

[26]  Patrick Flick,et al.  GOATOOLS: Tools for Gene Ontology , 2015 .

[27]  Michele Caselle,et al.  Statistics of shared components in complex component systems , 2017, 1707.08356.

[28]  Michael A. Saunders,et al.  Atomic Decomposition by Basis Pursuit , 1998, SIAM J. Sci. Comput..

[29]  Eugene V. Koonin,et al.  Gene Frequency Distributions Reject a Neutral Model of Genome Evolution , 2013, Genome biology and evolution.

[30]  Joshua L. Payne,et al.  No tradeoff between versatility and robustness in gene circuit motifs , 2016 .

[31]  Noah Fierer,et al.  Using network analysis to explore co-occurrence patterns in soil microbial communities , 2011, The ISME Journal.

[32]  Joshua S Weitz,et al.  A neutral theory of genome evolution and the frequency distribution of genes , 2012, BMC Genomics.

[33]  Elena Marchiori,et al.  Graph clustering with local search optimization: the resolution bias of the objective function matters most. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  Jun Yu,et al.  How many human genes can be defined as housekeeping with current expression data? , 2008, BMC Genomics.

[35]  G. Wagner,et al.  The road to modularity , 2007, Nature Reviews Genetics.

[36]  M. Wistrand,et al.  Proteome Organization in a Genome-Reduced Bacterium , 2009 .

[37]  J. Pereira-Leal,et al.  Modularity: Understanding the Development and Evolution of Natural Complex Systems , 2006 .

[38]  Christof Schütte,et al.  Modularity revisited: A novel dynamics-based concept for decomposing complex networks , 2014 .

[39]  Daniel Simberloff,et al.  The Assembly of Species Communities: Chance or Competition? , 1979 .

[40]  J. Cheverud,et al.  Modularity: genes, development and evolution. , 2016, Annual review of ecology, evolution, and systematics.

[41]  Hod Lipson,et al.  The evolutionary origins of modularity , 2012, Proceedings of the Royal Society B: Biological Sciences.

[42]  Carlos Prieto,et al.  Functional Integrative Levels in the Human Interactome Recapitulate Organ Organization , 2011, PloS one.

[43]  J. Thornton,et al.  Relationship between the tissue-specificity of mouse gene expression and the evolutionary origin and function of the proteins , 2005, Genome Biology.

[44]  Lyudmila F Gulyaeva,et al.  Regulatory mechanisms of microRNA expression , 2016, Journal of Translational Medicine.

[45]  Dirk M. Lorenz,et al.  The emergence of modularity in biological systems. , 2011, Physics of life reviews.

[46]  Ben Lehner,et al.  Tissue specificity and the human protein interaction network , 2009, Molecular systems biology.

[47]  Jane Bates,et al.  On form. , 2010, Nursing standard (Royal College of Nursing (Great Britain) : 1987).

[48]  D. Donoho,et al.  Atomic Decomposition by Basis Pursuit , 2001 .

[49]  Cheryl P. Andam,et al.  Genome Surfing As Driver of Microbial Genomic Diversity. , 2017, Trends in microbiology.

[50]  U. Alon,et al.  Spontaneous evolution of modularity and network motifs. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Andreas Wagner,et al.  Specialization Can Drive the Evolution of Modularity , 2010, PLoS Comput. Biol..

[52]  Jerzy Tiuryn,et al.  SIZE DISTRIBUTION OF GENE FAMILIES IN A GENOME , 2014 .

[53]  K. Sterelny.  Niche Construction, Developmental Systems and the Extended Replicator , 2001 .

[54]  Thierry Emonet,et al.  Understanding Modularity in Molecular Networks Requires Dynamics , 2009, Science Signaling.

[55]  Berend Snel,et al.  Quantifying modularity in the evolution of biomolecular systems. , 2004, Genome research.

[56]  L. Aravind,et al.  Comprehensive analysis of combinatorial regulation using the transcriptional regulatory network of yeast. , 2006, Journal of molecular biology.

[57]  D. Pe’er,et al.  Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data , 2003, Nature Genetics.