BACTJmOLOGICAL REVIEWS, June 1976, p. 469-524 Vol. 40, No. 2 Copyright 0 1976 American Society for Microbiology Printed in U.S.A. Comparative Aspects of Development and Differentiation in Actinomycetes L. V. KALAKOUTSKIIP* ArN NINA S. AGRE Microbiological Ontogenesis Research Unit, Institute ofBiochemistry, & Physiology ofMicroorganisms, USSR Academy ofScience, Poustchino on Oka, Moscow Region, 142292 USSR INTRODUCTION ............................................................. 469 Aims and Scope .............................................................. 469 Suitability of Various Types of Cultures for Studies of Development and Differen- tiation .................................................................. 470 Growth of Actinomycetes ................. ................................... 471 LIFE CYCLES IN THE ACTINOMYCETALES ....... ......................... 472 Generalized Scheme of Events Accompanying Reproduction ...... ............. 472 Multiplicity of Reproductive Patterns ......... ............................... 474 Rare and Unconfirmed Modes of Reproduction ........ ........................ 475 STATIC ASPECTS OF DIFFERENTIATION ........ .......................... 475 Differentiation within Colonies ............ .................................. 475 Differentiation of the Mycelium: Primary versus Secondary Mycelium ..... .... 476 Cellular Differentiation ................. .................................... 477 Amycelial Structures ........................................................ 479 Modes of Spore Formation ................ ................................... 481 Spores .................................................................. 483 Structure ................................................................. 483 Composition .............................................................. 484 Physiology ............................................................... 486 DYNAMIC ASPECTS OF DIFFERENTIATION ....... ......................... 487 Age-dependent Changes in Actinomycete Cells ....... ......................... 487 Environmental Conditions and Morphogenesis ....... ......................... 488 Metabolic Activity and Morphogenesis ......... ............................... 489 Environmental Factors in Control of Sporulation ....... ...................... 489 Nutritional limitations and sporulation: desiccation and other triggers ....... 489 Nutritional requirements for sporulation ........ ........................... 490 Supression of sporulation .............. .................................... 491 Sporulation under natural conditions ......... .............................. 491 Internal Factors in Control of Sporulation ...... ............................. 491 Variants and mutants with impaired differentiation ...... ................... 492 Sporulation and chromosomal genes ......... .............................. 493 Sporulation and plasmids ............. ..................................... 493 Proteolytic activity and sporulation and the question of RNA polymerase modifi- cation .................................................................. 493 Involvement of specific factors in regulation of sporulation ..... ............. 494 Spore Germination and Types of Dormancy Encountered ...... ................ 495 Constitutive dormancy of thermoresistant endospores and an overall picture of germination ............................................................ 496 Possibility of an alternative way for release from dormancy ..... ............ 496 Germination of exospores .............. .................................... 498 DIFFERENTIATION AND SECONDARY METABOLISM ...... ................ 500 Points of Similarity in Origin and Flow ......... ............................. 500 Prospects for Involvement of Antibiotics and Pigments in Regulation of Metabo- lism..................................................................... 503 Antibiotics and Their Components as Possible Building Blocks ..... ........... 504 LITERATURE CITED ......................................................... 506 INTRODUCTION taken as a group, would present difficulties, Aims and given the current state of our knowledge, al- Scope though they do pose intriguing and sometimes This paper is not going to suggest a new unique questions closely related to the area of model for studies in prokaryotic cell develop- developmental research. ment. It is believed that the Actinomycetales, I Present address: Microbial Ontogenesis Research Unit, nisms, USSR Academy of Science, Poustchino on Oka, Institute of Biochemistry and Physiology of Microorga- Moscow Region, 142292 USSR. 469 470 KALAKOUTSKII AND AGRE BACTERIOL. REV. The authors ofrecent reviews, dealing specif- screening for antibiotics and other products of ically or nonspecifically with particular prob- secondary metabolism. However, the very in- lems ofactinomycete development (69, 136, 235, teresting hypotheses linking secondary metab- 485), agree almost unanimously that develop- olism with differentiation (58, 449) were formu- mental studies with these forms lag behind lated using either fungi or endosporeforming those with viruses, aerobic sporeforming bacte- bacteria. These hypotheses, in our opinion, offer ria, and fungi. Whatever the reason, current very interesting perspectives for research, and trends of research with various organisms are consequently they merit extensive testing, spe- inconsistent, not only in terms of laboratory cifically with actinomycetes. Therefore, an at- techniques used, but also in the kinds of ques- tempt to examine the situation "from within tions asked, goals formulated, and ideas ex- the Actinomycetales" seemed timely (at least in ploited. Thus, periodic attempts to apply ap- helping some of our industrial colleagues to proaches becoming conventional with different realize that actinomycetes do not just grow and organisms appear merited. It is hoped that by produce everything possible, but they also so doing, the area of"lags" and potential break- somehow develop). throughs might become more precisely defined It is believed that the plan of this review will and comparative knowledge will be made more fit its aims without: (i) stating the basic prob- meaningful and thought provoking. lems, only to find supporting evidence insuffi- Now that the differences between eukaryotes cient, and (ii) describing organisms, one by one, and prokaryotes are understood, the old debate and reporting all relevant information, thus about whether the Actinomycetales are bacte- losing sight ofthe problems in the wealth ofless ria or fungi is definitely over. However, there relevant facts. are still reasons for comparing them with other Whenever there were no questions in our bacteria and fungi. minds, we used the generic names adopted in Chemical techniques, extensively employed the eighth edition ofBergey's Manual. In doubt- over the last two decades for characterization ful cases, generic names given in the original and identification purposes in microbiology and publications were retained. based mainly on determinations ofthe presence or absence of certain compounds, most often Suitability of Various Types of Cultures for confirmed the relatedness of the Actinomyce- Studies of Development and Differentiation tales to other bacteria ("true bacteria"). Using Information pertaining to development of ac- more complex features (wall structure, photo- tinomycetes currently stems mainly from stud- synthesis, gliding motility, endospore forma- ies that employ either submerged or surface tion, etc.) one can document differences be- cultures. Morphological and, very probably, tween gram-positive and gram-negative bacte- physiological and biochemical, manifestations ria. But what are the characteristic features of of differentiation in these types of cultures dif- the Actinomycetales, easily sensed by an ob- fer quite markedly. server, which support the idea of placing them To begin with, it is characteristic that most in a separate order, but which are not so easily differentiated representatives of the Actinomy- expressed in precise chemical terms? Are they cetales form hydrophobic aerial mycelia and not, to a large extent, the results of cellular spores in surface cultures. Although spore for- differentiation in these organisms? mation has repeatedly been reported to occur in Currently, Actinomycetales and fungi are be- submerged cultures, the spores and spore-bear- lieved to belong to different kingdoms of the ing structures formed under these conditions living world; it is inferred that their evolution- seem to differ morphologically and physiologi- ary separation is greater than that offishes and cally from these of surface cultures (cf. Spores, whales. Yet, striking examples ofsupposed con- below). Surface and submerged cultures might vergent evolution include not only mycelial or- differ also in the relative areas of cell contacts, ganization, but also general trends in reproduc- these tending to be more extensive in surface tive events. By comparing examples of analo- cultures. Cell crowding may well influence dif- gous differentiation, one might hope to learn ferentiation within hyphae, as seen, for in- about specific limits attainable at the prokar- stance, when submerged cultures grow in the yotic level. Relevant here also is the need to form of pellets. This influence is rather clearly understand the mechanisms allowing adapta- linked with changing gradients ofnutrient sup- tion to a different (terrestrial?) environment, in ply, accumulation