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Structures in 4D: a 'double tale' of biological accretion

"A double tale I'll tell. At one time one thing grew to be just one from many, at another many grew from one to be apart. Double the birth of mortal things, and double their demise." – On Nature , P. Strasb. Gr. Inv. 1665-6, Empedocles 1 The evolution of structure in biology is driven by accretion and change. Accretion brings together disparate parts to form bigger wholes. Change provides opportunities for growth and innovation. Here we review patterns and processes that are responsible for a ‘double tale’ of evolutionary accretion at various levels of complexity, from proteins and nucleic acids to building structures in cities. Parts are at first weakly linked and associate variously. As they diversify, they compete with each other and are selected for performance. The emerging interactions constrain their structure and associations. This causes parts to self- organize into modules with tight linkage. In a second phase, variants of the modules evolve and become new parts for a new generative cycle of higher- level organization. Evolutionary genomics and network biology support the ‘double tale’ of structural module creation 2 and validate an evolutionary principle of maximum abundance that drives the gain and loss of modules. Examples of structures in 4D include the origin of the ribosome, the proteome and metabolic networks 3-7 and the emergence of tall buildings in the Island of Manhattan 8 . 1 Janko R. (2004) Zeitschrift papyrologie epigraphik, 150 , 1-26 2 Mittenthal J.M., Caetano-Anollés D. and Caetano-Anollés G. (2012) Front. Genet., 3 , 147 3 Caetano-Anollés K. and Caetano-Anollés G. (2013) PloS One, 8 , e59300 4 Nasir A., Kim K.M. and Caetano-Anollés G. (2014) PLoS Comput. Biol., 10 , e1003452 5 Caetano-Anollés D. and Caetano-Anollés G. (2015) Comput. Struct. Biotech. J., 13 , 427-447. 6 Aziz M.F., Caetano-Anollés K. and Caetano-Anollés G. (2016) Sci. Rep., 6 , 25058 7 Nasir A., Kim K.M. and Caetano-Anollés G. (2017) Front. Microbiol., 8 , 1178 8 Schlomo A. and Lamson-Hall P. (2014) Marron Inst. Urban Mgmt. (New York Univ.), 14 , 1-48

F1000 Research Ltd

Gustavo Caetano-Anollés Derek Caetano-Anollés Kelsey Caetano-Anolles

2025

Title: Structures in 4D: a 'double tale' of biological accretion

Description:

"A double tale I'll tell.

At one time one thing grew to be just one from many, at another many grew from one to be apart.

Double the birth of mortal things, and double their demise.

" – On Nature , P.

Strasb.

Gr.

Inv.

1665-6, Empedocles 1 The evolution of structure in biology is driven by accretion and change.

Accretion brings together disparate parts to form bigger wholes.

Change provides opportunities for growth and innovation.

Here we review patterns and processes that are responsible for a ‘double tale’ of evolutionary accretion at various levels of complexity, from proteins and nucleic acids to building structures in cities.

Parts are at first weakly linked and associate variously.

As they diversify, they compete with each other and are selected for performance.

The emerging interactions constrain their structure and associations.

This causes parts to self- organize into modules with tight linkage.

In a second phase, variants of the modules evolve and become new parts for a new generative cycle of higher- level organization.

Evolutionary genomics and network biology support the ‘double tale’ of structural module creation 2 and validate an evolutionary principle of maximum abundance that drives the gain and loss of modules.

Examples of structures in 4D include the origin of the ribosome, the proteome and metabolic networks 3-7 and the emergence of tall buildings in the Island of Manhattan 8 .

1 Janko R.

(2004) Zeitschrift papyrologie epigraphik, 150 , 1-26 2 Mittenthal J.

, Caetano-Anollés D.

and Caetano-Anollés G.

(2012) Front.

Genet.

, 3 , 147 3 Caetano-Anollés K.

and Caetano-Anollés G.

(2013) PloS One, 8 , e59300 4 Nasir A.

, Kim K.

and Caetano-Anollés G.

(2014) PLoS Comput.